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array_files[0]=new Array(0,1,"http://webs.uvigo.es/c04/webc04/etologia/noticias.html","2012-02-09","81K","Noticias - Sociedad Española de Etología    ","",""," Noticias - Sociedad Española de Etología label label label Inicio Quiénes somos Noticias Hacerse socio Publicaciones Enlaces Contactar Área privada XXV Aniversario Congreso Nacional e Iberoamericano de Etología XXIX International Ethological Conference Enseñanza de la Etología en la Universidad Vocabulario etológico Documentales Bicentenariode Darwin Concurso Fotográfico Investigación Noticias Disponible para descarga la versión íntegra del libro Adaptive Behaviour: Understanding the Human Animal, de Manuel Soler 09/02/2012 Autor: Manuel Soler. La aceptación por parte de los etólogos de que el comportamiento, al igual que cualquier otra característica de los seres vivos, es el resultado de la evolución por selección natural supuso la implantación de un enfoque evolutivo que dio lugar al nacimiento de la llamada ecología del comportamiento, que se convirtió en una de las ciencias más importantes e influyentes de la biología evolutiva... Ir a la página de Publicaciones... XIV Congreso Nacional y XI Iberoamericano de la Sociedad Española de Etología Sevilla, 11 al 15 de Septiembre 2012 29/09/2011 El XIV Congreso Nacional y XI Iberoamericano de la Sociedad Española de Etología (SEE) se celebrará en Sevilla del martes 11 al viernes 14 de Septiembre de 2012, organizado por la Estación Biológica de Doñana y la Universidad de Sevilla. La Estación Biológica de Doñana (EBD) es un instituto público de investigación perteneciente a la Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC). La EBD se creó en 1965 como un instituto dedicado al estudio de la ecología terrestre y más tarde amplió su ámbito de conocimiento a la biología evolutiva y la ecología del comportamiento. El Instituto está constituido por su sede principal en Sevilla y dos estaciones de campo, la Reserva Biológica de Doñana y la Estación de Campo de Roblehondo (Parque Natural de las Sierras de Cazorla, Segura y las Villas). La Estación Biológica de Doñana cuenta con una sólida tradición en estudios sobre etología y ecología del comportamiento, tanto desde una perspectiva evolutiva básica como aplicada a la conservación de la fauna salvaje. Se ha Programado una visita al P. N. de Doñana el sábado día 15. Más información: Ir a la página del XIV Congreso... Descubriendo el comportamiento animal en el programa Reserva Natural, en Radio 5 26/09/2011 Descubriendo el comportamiento animal en el programa Reserva Natural, en Radio 5. Josefina Maestre ha tenido esta semana de invitado a Juan Carranza que junto Alberto Jose Redondo socio de la Asociación Española de Cine e imagen Científicos, dirigen y producen la serie “Descubriendo el Comportamiento animal” la serie que emite actualmente La 2 de TVE, de cuyos contenidos habla Juan Carranza, presidente de la Sociedad Española de Etología y uno de los responsables del proyecto. Ir a la página de Reserva Natural... Nueva emisión en La2 de TVE de la serie documental “Descubriendo el comportamiento animal” 24/08/2011 Comienza una nueva emisión en TVE de los documentales de la serie DESCUBRIENDO EL COMPORTAMIENTO ANIMAL producidos por la SEE. La emisión será a partir del próximo viernes día 26 de Agosto, a las 14:30h por La2 de TVE, de lunes a viernes. Se emitirán 21 capítulos, 12 que ya emitieron el pasado año y 9 capítulos nuevos que se han producido durante el 2010 y que no han sido emitidos hasta el momento. Disponible para descarga el libro Etología - Introducción a la Ciencia del Comportamiento, J. Carranza (1994) 08/06/2011 Está ya disponible para descarga libre en la sección de publicaciones el libro Etología. Introducción a la Ciencia del Comportamiento - Juan Carranza, Publ. Universidad de Extremadura, 1994, en formato PDF (9.6 MBytes). Ir a la página de descarga... Clausura del Máster Universitario en Etología 2010-2011 15/04/2011 Se ha clausurado el Máster en Etología por la Universidad de Córdoba. El acto estuvo presidido por la Directora del Secretariado de Másteres y Prospectiva de la UCO, Mar Delgado, la Vicedecana de Investigación, Relaciones Internacionales y Movilidad de la Facultad de Ciencias de la UCO, Mª Teresa Roldán y los directores académicos del Máster y Profesores del Departamento de Zoología, Luis Arias de Reyna y Pilar Recuerda. Los 26 alumnos que han cursado este Máster en su primera edición (véase foto más abajo), en el curso 2010-2011, recogieron un diploma acreditativo. Los estudiantes, pertenecientes a ocho comunidades autónomas, han recibido clases y conferencias de una gran cantidad de especialistas en Etología de nuestro país, en un Máster que ha sido patrocinado por la Consejería de Medio Ambiente de la Junta de Andalucía y promovido por la Sociedad Española de Etología. Leer más... Ya está disponible el DVD de la serie documental Descubiendo el comportamiento animal 17/09/2010 Se han editado en DVD los 12 capítulos de 5 minutos de la premiada serie documental Descubiendo el comportamiento animal producida por Alberto José Redondo Villa y Juan Carranza Almansa. Todo el material de la serie es original, tanto las imágenes como el grafismo, la música especialmente compuesta para la serie, el sonido ambiente, la locución, etc. Todo el material es original, tanto las imágenes como el grafismo de la cabecera, la música compuesta e interpretada expresamente para la serie, el sonido ambiente, la locución, etc. En este sentido se cuenta con la participación en la serie de Antonio Torres Porras, compositor y músico de la Orquesta Nacional de España, y de José Ángel de Juanes que se encarga de la locución, aportando su inconfundible calidad de voz que realza el valor comunicativo de cualquier producción documental. La serie documental está respaldada por la Asociación Española de Cine Científico (ASECIC). La serie, ha contado con la colaboración de FECYT, las Universidades de Córdoba y Extremadura, el CSIC, la Junta de Extremadura y Red Eléctrica de España. Este DVD se entregó a todos los socios de la SEE participantes en el congreso que se celebó entre los días 21 y 24 de septiembre de 2010 en Ciudad Real (España), así como a todos aquellos participantes que se hicieron socios de la SEE durante el congreso. Más información acerca de la serie documental aquí y aquí. Máster Universitario en Etología 2010-2011 02/06/2010 El próximo curso, 2010-2011, se comenzará a impartir en la Universidad de Córdoba, el Máster Universitario en Etología, promovido por la Sociedad Española de Etología. El Máster pretende proporcionar una formación científica avanzada que permita a los alumnos conocer el comportamiento animal e incluirlo en el contexto de las características biológicas que, fácilmente moldeables, proporcionan una base evolutiva y ecológica que permita un uso más racional de los animales. Mediante los dos perfiles que se ofertan, los alumnos podrán adquirir una base formativa sólida para iniciar una carrera investigadora (Perfil Investigador) o bien para su incorporación al mercado de trabajo como profesional (Perfil Profesional). La duración es de 60 créditos ECTS agrupados en tres módulos (Metodología, Especialización y Trabajo fin de Máster) que se cursarán en un año. Para más información: Web de la Universidad de Córdoba (UCO), dentro del área Recursos Naturales y Gestión Sostenible. Web del Distrito Único Andaluz (DUA). Contacto: e-mail: masteretologia@uco.es Si lo desea, puede descargar los folletos publicitarios (en formato PDF) haciendo click sobre cada una de las siguientes imágenes: Descargar Folleto publicitario del Máster 2010-2011 (anverso) Descargar Folleto publicitario del Máster 2010-2011 (reverso) Comienza a emitirse en TVE la serie documental “Descubriendo el comportamiento animal” 21/04/2010 El lunes 26 de Abril de 2010 se iniciará la emisión en La 2 de TVE de la serie documental Descubriendo el Comportamiento Animal, producida por Alberto José Redondo Villa (Profesor del Departamento de Zoología de la Universidad de Córdoba) y Juan Carranza Almansa (Catedrático del Área de Zoología de la Universidad de Extremadura, Director de la Cátedra de Recursos Cinegéticos y Piscícolas de la Universidad de Córdoba y Presidente de la Sociedad Española de Etología). Cada capítulo será emitido en torno a las 18:40-18:45 horas, entre Grandes Documentales y El Hombre y la Tierra. La serie consta por el momento de 12 capítulos que consisten en documentales de 5 minutos de duración que presentan una investigación concreta sobre comportamiento animal. La realización de este trabajo surge como una iniciativa de la Sociedad Española de Etología, en la necesidad de contribuir a la divulgación de los trabajos científicos llevados a cabo por investigadores de prestigio en el campo de la etología. El trabajo va enfocado a ayudar a comprender, al público en general, por qué los animales se comportan de una determinada manera, en una situación concreta, y cómo este comportamiento se debe a la actuación de la selección natural, responsable de que las especies se mantengan tal y como son, para lo cual es necesario que continúen llevando a cabo sus comportamientos naturales. Además, siempre los temas incluyen elementos de conservación, a los cuales se llega de un modo natural tras el conocimiento de comportamientos sorprendentes que pretenden captar la atención del espectador. La metodología de trabajo consiste en la realización de un guión de cada capítulo temático, que se lleva a cabo entre los investigadores expertos en cada área y los productores de la serie, Alberto José Redondo Villa y Juan Carranza Almansa, así como la grabación de las imágenes adecuadas en el tiempo y lugar y la realización del documental a cargo del profesor Alberto José Redondo Villa. Todo el material es original, tanto las imágenes como el grafismo de la cabecera, la música compuesta e interpretada expresamente para la serie, el sonido ambiente, la locución, etc. En este sentido se cuenta con la participación en la serie de Antonio Torres Porras, compositor y músico de la Orquesta Nacional de España, y de José Ángel de Juanes que se encarga de la locución, aportando su inconfundible calidad de voz que realza el valor comunicativo de cualquier producción documental. La serie documental está respaldada por la Asociación Española de Cine Científico (ASECIC). La serie, ha contado con la colaboración de FECYT, las Universidades de Córdoba y Extremadura, el CSIC, la Junta de Extremadura y Red Eléctrica de España. A continuación se presenta una sinopsis de los doce capítulos de la serie DESCUBRIENDO EL COMPORTAMIENTO ANIMAL: Capítulo 1: Pequeñas esclavistas. Basado en los trabajos del Dr. Alberto Tinaut. Muestra el comportamiento de captura de esclavas en una especie de hormigas en Sierra Nevada. Capítulo 2: Mensajes de colores. ¿Por qué tienen colores llamativos las aves? El investigador Juan Carlos Senar ha descubierto que diferentes colores tienen distintos mensajes, el amarillo intenso significa salud y el negro agresividad. Capítulo 3: La paradoja de los huevos azules. El Dr Juan Moreno ha descubierto que mediante los colores de sus huevos las hembras pueden comunicar su calidad a los machos. Los huevos más azules animan a los machos a trabajar más, pues indican que su pareja se encuentra en buenas condiciones. Capítulo 4: Seductores perfumados. Los Dres. Pilar López y José Martín aportan sus trabajos sobre selección sexual en lagartijas y el papel de señales químicas en la comunicación entre rivales y parejas. Capítulo 5: Tarjetas de visita. Comunicación química en el topillo nival. En él participa el Dr. Juanjo Luque Larena. Capítulo 6: Fecundación a la carta. Este capítulo se basa en las investigaciones llevadas a cabo por el Dr. Juan Carranza sobre selección sexual en el ciervo. Los machos luchan pero al final son las hembras las que tienen la última palabra. Capítulo 7: Amar peligrosamente. El canibalismo en las tarántulas es el tema de estudio en este documental. Mediante nidos adaptados se ha filmado la vida íntima de estos arácnidos desentrañando las motivaciones de este espectacular comportamiento que ha sido motivo de estudio por parte del Dr. Jordi Moya. Capítulo 8: Coraje de madres. Rodado en Asturias, trata sobre el infanticidio en el oso pardo y su problemática de conservación. Las osas en la cordillera cantábrica se enfrentan a veces al comportamiento infanticida de machos en celo. El documental se basa en las investigaciones de un equipo dirigido por el Dr. Miguel Delibes. Capítulo 9: Olvido afortunado. Se basa en las investigaciones del Dr. Mario Díaz sobre el modo en que los ratones almacenan bellotas y, como consecuencia de algunos olvidos, hacen posible la reproducción de las encinas. Capítulo 10: Paternidad conflictiva. Trata sobre la competencia espermática en libélulas, basado en las investigaciones del Dr. Adolfo Cordero. Capítulo 11: Ayudantes de cría. La cría cooperativa en el rabilargo, basado en los trabajos de los Dres. Carlos de la Cruz y Juliana Valencia. Muestra como ciertos individuos, en lugar de criar por sí mismos, ayudan a sacar adelante a los pollos de otros. Capítulo 12: Buscando el paraíso. Trata sobre el comportamiento de dispersión en el lince ibérico, según recientes publicaciones de Eloy Revilla de la EBD, y de la problemática de su conservación, incluyendo las acciones in situ y ex situ. Contactos para prensa: Alberto José Redondo Villa Juan Carranza Almansa FALLO DEL I CONCURSO DE FOTOGRAFÍA «COMPORTAMIENTO ANIMAL» XXVANIVERSARIODELASOCIEDADESPAÑOLADEETOLOGÍA 24/10/2009 A partir de las 55 fotografías seleccionadas como finalistas, el jurado del concurso de fotografía sobre “comportamiento animal”, compuesto por:: Presidente: Juan Carranza Vice-presidente: Juan Moreno Secretario: Juan Carlos Senar Expertos en fotografía de naturaleza: Jerónimo Torres y Jordi Vidal F. Ha decidido otorgar los siguientes premios:... Ampliar noticia... Page Up FALLO DEL JURADO DE LA XXII CONVOCATORIA DE LOS PRISMAS CASA DE LAS CIENCIAS A LA DIVULGACIÓN 28/09/2009 Una serie de documentales que descubre el como y el por qué de los comportamientos de algunas especies animales, un libro que analiza las creencias e ideas aparentemente científicas despertando el sentido crítico y el escepticismo del lector, un artículo periodístico sobre el origen del universo, y un texto inédito sobre la metamorfosis de los insectos obtuvieron los Prismas de Bronce en esta XXII convocatoria. El Prisma Especial del Jurado, dotado por PharmaMar grupo Zeltia con 9.000 euros, fue para a la revista Mètode, de la Universitat de Valencia. Cuadro de honor, 2009: Mejor trabajo multimedia: Descubriendo el comportamiento animal, serie documental original de Alberto José Redondo Villa y Juan Carranza Almansa. Mejor libro editado:Por qué creemos en cosas raras. Pseudociencia, superstición y otras confusiones de nuestro tiempo, de Alba Editorial y original de Michael Shermer. Mejor artículo periodístico:El origen del todo, de Silbia López de Lacalle, y publicado en Popular Science. Mejor texto original e inédito: Vivir dos vidas. Un viaje por la metamorfosis de los insectos”, de Xavier Bellés. Prisma Especial del Jurado: a la revista Mètode, de la Universitat de Valencia. Composición del Jurado: Presidente: D. Vladimir Francisco de Semir, Universitat Pompeu Fabra. Compuesto además por: Dña. Patricia Fernández de Lis, periodista de Público, D. Alejandro Fernández de las Peñas, director de CosmoCaixa Madrid, D. Joaquín Fernández Pérez, catedrático de Biología Celular de la Universidad Autónoma de Madrid, D. Fernando Mugarza, Director de Comunicación de PharmaMar Grupo Zeltia, D. José Antonio de Lorenzo Pardo, IES Salvador de Madariaga (A Coruña), D. Raúl Romar, periodista de La Voz de Galicia. D. Xosé Antón Fraga Vázquez, Director de los Museos Científicos Coruñeses, actuó como Secretario. RELACIÓN DE PREMIOS OTORGADOS Modalidad de trabajos multimedia El Prisma de Bronce al mejor trabajo multimedia destinado a la divulgación científica, y el premio dotado con seis mil euros, fue otorgado a la serie documental titulada Descubriendo el comportamiento animal, original de Alberto José Redondo Villa y Juan Carranza Almansa, por su originalidad, capacidad de síntesis y atractivo y por la importancia que tiene la implicación de los investigadores en la divulgación científica. Modalidad de libros editados en 2008 Se decidió otorgar el Prisma al mejor libro de divulgación científica editado en España en 2008 al titulado Por qué creemos en cosas raras. Pseudociencia, superstición y otras confusiones de nuestro tiempo, de Alba Editorial y original de Michael Shermer, porque traslada a la sociedad la necesidad de adoptar posturas analíticas y críticas frente a la pseudociencia y la irracionalidad. Modalidad de artículos periodísticos El Prisma al mejor artículo periodístico de divulgación científica publicado durante el año 2008, dotado con seis mil euros, fue otorgado al trabajo El origen del todo, de Silbia López de Lacalle y publicado en Popular Science, por la habilidad para hacer comprensible un tema conocido pero tan complejo como el origen del cosmos desde una perspectiva muy sugestiva y completa. Modalidad de textos originales e inéditos Se decidió otorgar el Prisma de Bronce al mejor texto original e inédito de divulgación científica, dotado con seis mil euros y la publicación de la primera edición, al que lleva por título Vivir dos vidas. Un viaje por la metamorfosis de los insectos , del que es autor Xavier Bellés, por la calidad de la narración, rigor y originalidad del texto, tema elegido y el esfuerzo divulgativo. Premio especial del Jurado Se decidió otorgar el Prisma Especial del Jurado, dotado por PharmaMar grupo Zeltia con 9.000 euros, a la revista Mètode, de la Universitat de Valencia, por el esfuerzo continuado de divulgación científica de calidad y por la implicación de una universidad en la promoción de la cultura cientifica. Fuente: Ver Nota de Prensa Page Up PRESENTADOS A LA COMUNIDAD CIENTÍFICA LOS NUEVOS CAPÍTULOS DE LA SERIE “DESCUBRIENDO EL COMPORTAMIENTO ANIMAL” Los tres primeros capítulos de la serie, producida y coordinada por la Sociedad Española de Etología, obtuvieron en 2008 el premio del ÁREA INVESTIGACIÓN en el XXV Certamen Unicaja de Cine, Bienal Internacional de Cine Científico. En el salón de actos del CENTRO DE CIENCIAS MEDIOAMBIENTALES, del Consejo superior de Investigaciones Científicas, se han presentado a la comunidad científica 4 nuevos capítulos de la serie “Descubriendo el Comportamiento Animal” la serie que coordina y produce la Sociedad Española de Etología y que cuenta ya con 7 capítulos terminados. Al acto asistieron Alberto Redondo Villa (director y realizador), Juan Carranza Almansa (productor y presidente de la Sociedad Española de Etología), el locutor de la serie José Ángel de Juanes y el músico Antonio Torres Porras. Los nuevos capítulos han sido posibles gracias a la financiación del Proyecto Divulgación de descubrimientos sobre comportamiento animal en el XXV aniversario de la Sociedad Española de Etología, en la Convocatoria Ayudas para el Fomento de la Cultura Científica y Tecnológica 2009 de FECYT, Ministerio de Ciencia e Innovación. A finales de año los 12 capítulos de la serie estarán terminados, en cada uno de ellos se muestran los resultados de las investigaciones de científicos de la Sociedad Española de Etología, que desarrollan sus trabajos en el CSIC y en varias universidades españolas. En los cinco minutos que dura cada uno de ellos podemos comprender el cómo y el porqué del comportamiento de diferentes especies en las situaciones de su vida diaria. La serie rodada en alta definición y con una excelente calidad de imagen, esta obteniendo un enorme reconocimiento no sólo en la comunidad científica sino en el mundo del audiovisual. Su inusual duración, cinco minutos por capítulo, no impide que lo que quieren contar sus autores quede perfectamente comprendido por el espectador, siendo por esto una excelente herramienta para el mundo educativo así como para el ciudadano en general, ya que brinda una posibilidad de acercarse a un conocimiento desconocido por la mayoría sobre el comportamiento de los animales en su entorno natural. Tras la proyección un interesante debate con los etólogos y ecólogos que acudieron al acto, quienes reconocieron de la exactitud de la serie y el rigor científico que mantiene en la totalidad de los capítulos, mostrando además descubrimientos científicos muy recientes, que además permiten conocer el trabajo de los científicos fuera del laboratorio. Los doce capítulos: Capítulo 1: Mensajes de colores. ¿Por qué tienen colores llamativos las aves? El investigador Juan Carlos Senar del Museo de Zoología de Barcelona ha descubierto que diferentes colores tienen distintos mensajes, el amarillo intenso significa salud y el negro agresividad. Capítulo 2: La paradoja de los huevos azules. Las hembras de aves no tienen colores llamativos, pero un estudio científico realizado por el equipo del Dr Juan Moreno del Museo Nacional de Ciencias Naturales ha descubierto que mediante los colores de sus huevos pueden comunicar su calidad a los machos. Los huevos más azules animan a los machos a trabajar más, pues indican que su pareja se encuentra en buenas condiciones. Capítulo 3: Amar peligrosamente. El canibalismo en las tarántulas es el tema de estudio en este documental. Mediante nidos adaptados se ha filmado la vida íntima de estos arácnidos desentrañando las motivaciones de este espectacular comportamiento que ha sido motivo de estudio por parte del Dr. Jordi Moya de la Estación Experimental de Zonas Áridas de Almería. Capítulo 4: Fecundación a la carta. Este capítulo se basa en las investigaciones llevadas a cabo por el Dr. Juan Carranza (Universidad de Extremadura) sobre selección sexual en el ciervo. Los machos luchan pero al final son las hembras las que tienen la última palabra. Capítulo 5: Olvido afortunado. Se basa en las investigaciones del Dr. Mario Díaz (CISIC, Madrid) sobre el modo en que los ratones almacenan bellotas y, como consecuencia de algunos olvidos, hacen posible la reproducción de las encinas. Capítulo 6: Ayudantes de cría. La cría cooperativa en el rabilargo, basado en los trabajos de los Dres. Carlos de la Cruz (Universidad de Extremadura) y Juliana Valencia (CSIC). Muestra como ciertos individuos, en lugar de criar por sí mismos, ayudan a sacar adelante a los pollos de otros. Capítulo 7: Pequeñas esclavistas. Basado en los trabajos del Dr. Alberto Tinaut de la Universidad de Granada. Muestra el comportamiento de captura de esclavas en una especie de hormigas en Sierra Nevada. Capítulo 8: Seductores perfumados. Los Dres. Pilar López y José Martín (CSIC, Madrid) aportan sus trabajos sobre selección sexual en lagartijas y el papel de señales químicas en la comunicación entre rivales y parejas. Capítulo 9: Paternidad conflictiva. Trata sobre la competencia espermática en libélulas, basado en las investigaciones del Dr. Adolfo Cordero (Universidad de Vigo). Capítulo 10: Coraje de madres. Las osas en la cordillera cantábrica se enfrentan a veces al comportamiento infanticida de machos en celo. El documental se basa en las investigaciones de un equipo dirigido por el Dr.Miguel Delibes (EBD, CSIC). Capítulo 11: Tarjetas de visita. Comunicación química en el topillo nival. En él participa el Dr. Juanjo Luque Larena (Palencia). Capítulo 12: Dispersión en el lince ibérico. En este documental aporta sus investigaciones el Dr. Eloy Revilla de la Estación Biológica de Doñana (CSIC). El equipo de la serie pretende ampliar la duración de algunos de los capítulos, pensado en poder llegar al gran público con un formato de media hora a través de las televisiones. La producción de estos nuevos documentales, con un elevado coste, necesita nueva financiación; en su búsqueda se han unido el equipo de la serie, la Sociedad Española de Etología y la Asociación Española de Cine e Imagen Científicos. Contacto: Alberto José Redondo Villa: ba1revia@uco.es, Tel.: +34.699.509.232 Juan Carranza Almansa: carranza@unex.es, Tel: +34.657 391273 Más información y cortes de los documentales: http://www.asecic.org http://www.etologia.org De izquierda a derecha: Antonio Torres Porras (músico), Alberto Redondo Villa (director y realizador), Juan Carranza Almansa (presidente de la Sociedad Española de Etología e impulsor de la serie) y José Angel de Juanes (locutor). English version... Page Up 55 fotos finalistas del I Concurso Fotográfico El jurado ya ha seleccionado las fotografías finalistas Desde aquí queremos agradecer a todos los concursantes su participación en este I Concurso de Fotografía de la SEE, y aprovechar para felicitar a los finalistas, a los que les deseamos mucha suerte para alcanzar uno de los tres premios disponibles. Leer más... Page Up LA SERIE DOCUMENTAL COMPORTAMIENTO ANIMAL PRODUCIRÁ NUEVOS CAPITULOS GRACIAS A LA FINANCIACIÓN DE LA FECYT La serie cuyos tres primeros capítulos obtuvieron el premio de la sección de investigación de la XXV Bienal de Cine Científico Unicaja, celebrada en Ronda en noviembre de 2008. Con una producción atípica en el mundo audiovisual actual, con un formato muy corto, se convertirá sin duda en una herramienta imprescindible para profesores de biología de los diferentes niveles educativos. Se trata de un proyecto presentado por Juan Carranza Almansa (Presidente de la Sociedad Española de Etología) para contribuir a la financiación de la serie documental que realiza Alberto José Redondo Villa (profesor de la Universidad de Córdoba y socio de ASECIC). La Fundación Española para la Ciencia y la Tecnología FECYT, en su convocatoria de ayudas 2009 Programa de Cultura Científica y de la Innovación, ha aprobado la financiación del proyecto titulado DIVULGACIÓN DE DESCUBRIMIENTOS SOBRE COMPORTAMIENTO ANIMAL EN EL XXV ANIVERSARIO DE LA SOCIEDAD ESPAÑOLA DE ETOLOGÍA con referencia FCT-09-504. Permitirá la producción de más de 12 capítulos de diseñados de forma ágil y con una duración de no más de cinco minutos que nos permitirán conocer y entender el cómo y el porqué del comportamiento de alguna de las especies con las que los humanos compartimos el Planeta Tierra. Leer más... Page Up I CONCURSO DE FOTOGRAFÍA «COMPORTAMIENTO ANIMAL» 2009 Ya se ha cerrado el plazo de inscripción del concuro fotográfico para la edición del 2009. Cumplimos 25 años. En el año 2009, la SEE cumple 25 años. La conmemoración de este aniversario se centrará en la difusión de la ciencia. Las siguientes actividades conmemorativas tendrán el objetivo de potenciar la divulgación de los trabajos científicos llevados a cabo por investigadores de nuestra Sociedad en el campo del comportamiento animal: Concurso de Fotografía sobre el tema “Comportamiento animal” Publicación del libro titulado “ESTUDIOS SOBRE COMPORTAMIENTO ANIMAL” Continuación de la serie documental “DESCUBRIENDO EL COMPORTAMIENTO ANIMAL” Estrenamos nueva página web. Page Up Acta Ethologica The new Journal of SEE. Índice de impacto (Impact Factor): 0.667 (2007) Acta Ethologica es la revista oficial de la Sociedad Española de Etología, substituyendo a la anterior publicación Etología. Acta Ethologica se publica conjuntamente con la Sociedad Portuguesa de Etología y el Instituto Superior de Psicología Aplicada. Acta Ethologica enfatiza estudios integrativos donde se analicen tanto los mecanismos como la función y evolución del comportamiento. Aspectos de especial interés incluyen la plasticidad adaptativa del comportamiento, variaciones inter-individuales y geográficas del comportamiento, y los procesos evolutivos que regulan el comportamiento y sus funciones. Si has cambiado de correo electrónico, contacta con la SEE: muchos de los contactos desde la SEE se realizan actualmente por correo electrónico. Sin embargo, se devuelven numerosos mensajes, sin duda porque las direcciones de correo-e cambian muy a menudo. Por favor, contacta con la sede si has cambiado recientemente tu dirección. Page Up Contactar con la S.E.E. © Copyright 2002-2009 SEE Aviso Legal     ");
array_files[1]=new Array(0,1,"http://webs.uvigo.es/c04/webc04/etologia/index.html","2012-02-09","35K","Sociedad Española de Etología    ","",""," Sociedad Española de Etología label label label Inicio Quiénes somos Noticias Hacerse socio Publicaciones Enlaces Contactar Área privada XXV Aniversario Congreso Nacional e Iberoamericano de Etología XXIX International Ethological Conference Enseñanza de la Etología en la Universidad Vocabulario etológico Documentales Bicentenariode Darwin Concurso Fotográfico Investigación Disponible para descarga la versión íntegra del libro Adaptive Behaviour: Understanding the Human Animal, de Manuel Soler 09/02/2012 Autor: Manuel Soler. La aceptación por parte de los etólogos de que el comportamiento, al igual que cualquier otra característica de los seres vivos, es el resultado de la evolución por selección natural supuso la implantación de un enfoque evolutivo que dio lugar al nacimiento de la llamada ecología del comportamiento, que se convirtió en una de las ciencias más importantes e influyentes de la biología evolutiva... Ir a la página de Publicaciones... XIV Congreso Nacional y XI Iberoamericano de la Sociedad Española de Etología 29/09/2011 Sevilla, 11 al 15 de Septiembre 2012 El XIV Congreso Nacional y XI Iberoamericano de la Sociedad Española de Etología (SEE) se celebrará en Sevilla del martes 11 al viernes 14 de Septiembre de 2012, organizado por la Estación Biológica de Doñana y la Universidad de Sevilla. La Estación Biológica de Doñana (EBD) es un instituto público de investigación perteneciente a la Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC). La EBD se creó en 1965 como un instituto dedicado al estudio de la ecología terrestre y más tarde amplió su ámbito de conocimiento a la biología evolutiva y la ecología del comportamiento. El Instituto está constituido por su sede principal en Sevilla y dos estaciones de campo, la Reserva Biológica de Doñana y la Estación de Campo de Roblehondo (Parque Natural de las Sierras de Cazorla, Segura y las Villas). La Estación Biológica de Doñana cuenta con una sólida tradición en estudios sobre etología y ecología del comportamiento, tanto desde una perspectiva evolutiva básica como aplicada a la conservación de la fauna salvaje. Se ha Programado una visita al P. N. de Doñana el sábado día 15. Más información: Ir a la página del XIV Congreso... Descubriendo el comportamiento animal en el programa Reserva Natural, en Radio 5 26/09/2011 Descubriendo el comportamiento animal en el programa Reserva Natural, en Radio 5. Josefina Maestre ha tenido esta semana de invitado a Juan Carranza que junto Alberto Jose Redondo socio de la Asociación Española de Cine e imagen Científicos, dirigen y producen la serie “Descubriendo el Comportamiento animal” la serie que emite actualmente La 2 de TVE, de cuyos contenidos habla Juan Carranza, presidente de la Sociedad Española de Etología y uno de los responsables del proyecto. Ir a la página de Reserva Natural... Nueva emisión en La2 de TVE de la serie documental “Descubriendo el comportamiento animal” 24/08/2011 Comienza una nueva emisión en TVE de los documentales de la serie DESCUBRIENDO EL COMPORTAMIENTO ANIMAL producidos por la SEE. La emisión será a partir del próximo viernes día 26 de Agosto, a las 14:30h por La2 de TVE, de lunes a viernes. Se emitirán 21 capítulos, 12 que ya emitieron el pasado año y 9 capítulos nuevos que se han producido durante el 2010 y que no han sido emitidos hasta el momento. Disponible para descarga el libro Etología - Introducción a la Ciencia del Comportamiento, J. Carranza (1994) 08/06/2011 Está ya disponible para descarga libre en la sección de publicaciones el libro Etología. Introducción a la Ciencia del Comportamiento - Juan Carranza, Publ. Universidad de Extremadura, 1994, en formato PDF (9.6 MBytes). Ir a la página de descarga... Clausura del Máster Universitario en Etología 2010-2011 15/04/2011 Se ha clausurado el Máster en Etología por la Universidad de Córdoba. El acto estuvo presidido por la Directora del Secretariado de Másteres y Prospectiva de la UCO, Mar Delgado, la Vicedecana de Investigación, Relaciones Internacionales y Movilidad de la Facultad de Ciencias de la UCO, Mª Teresa Roldán y los directores académicos del Máster y Profesores del Departamento de Zoología, Luis Arias de Reyna y Pilar Recuerda. Los 26 alumnos que han cursado este Máster en su primera edición (véase foto más abajo), en el curso 2010-2011, recogieron un diploma acreditativo. Los estudiantes, pertenecientes a ocho comunidades autónomas, han recibido clases y conferencias de una gran cantidad de especialistas en Etología de nuestro país, en un Máster que ha sido patrocinado por la Consejería de Medio Ambiente de la Junta de Andalucía y promovido por la Sociedad Española de Etología. Leer más... Ya está disponible el DVD de la serie documental Descubiendo el comportamiento animal Se han editado en DVD los 12 capítulos de 5 minutos de la premiada serie documental Descubiendo el comportamiento animal producida por Alberto José Redondo Villa y Juan Carranza Almansa. Todo el material de la serie es original, tanto las imágenes como el grafismo, la música especialmente compuesta para la serie, el sonido ambiente, la locución, etc. Este DVD se entregó a todos los socios de la SEE participantes en el congreso que se celebró entre los días 21 y 24 de septiembre de 2010 en Ciudad Real (España), así como a todos aquellos participantes que se hicieron socios de la SEE durante el congreso. Leer más... Publicado un nuevo libro por la SEE: Estudios sobre Comportamiento Animal XXV años de la Sociedad Española de Etología Acaba de ver la luz el libro Estudios sobre comportamiento animal - XXV años de la Sociedad española de Etología patrocinado por la Universidad de Extremadura y por la SEE en conmemoración de los XXV años de la Sociedad Española de Etología Este libro recopila una serie de artículos publicados en la revista Quercus sobre comportamiento animal por varios investigadores de la Sociedad Española de Etología. Durante la celebración del XIII Congreso de Etología que se celebró del 21 al 24 de septiembre en Ciudad Real (España), se entregó un ejemplar del libro y del DVD de la serie documental Descubiendo el comportamiento animal a todos los socios de la SEE, así como a todos aquellos participantes que se hicieron socios de la misma durante el congreso. Leer más... >> Ver entradas antiguas << Contactar con la S.E.E. © Copyright 2002-2009 SEE Aviso Legal     ");
array_files[2]=new Array(0,1,"http://webs.uvigo.es/c04/webc04/etologia/","2012-02-09","35K","Sociedad Española de Etología    ","",""," Sociedad Española de Etología label label label Inicio Quiénes somos Noticias Hacerse socio Publicaciones Enlaces Contactar Área privada XXV Aniversario Congreso Nacional e Iberoamericano de Etología XXIX International Ethological Conference Enseñanza de la Etología en la Universidad Vocabulario etológico Documentales Bicentenariode Darwin Concurso Fotográfico Investigación Disponible para descarga la versión íntegra del libro Adaptive Behaviour: Understanding the Human Animal, de Manuel Soler 09/02/2012 Autor: Manuel Soler. La aceptación por parte de los etólogos de que el comportamiento, al igual que cualquier otra característica de los seres vivos, es el resultado de la evolución por selección natural supuso la implantación de un enfoque evolutivo que dio lugar al nacimiento de la llamada ecología del comportamiento, que se convirtió en una de las ciencias más importantes e influyentes de la biología evolutiva... Ir a la página de Publicaciones... XIV Congreso Nacional y XI Iberoamericano de la Sociedad Española de Etología 29/09/2011 Sevilla, 11 al 15 de Septiembre 2012 El XIV Congreso Nacional y XI Iberoamericano de la Sociedad Española de Etología (SEE) se celebrará en Sevilla del martes 11 al viernes 14 de Septiembre de 2012, organizado por la Estación Biológica de Doñana y la Universidad de Sevilla. La Estación Biológica de Doñana (EBD) es un instituto público de investigación perteneciente a la Agencia Estatal Consejo Superior de Investigaciones Científicas (CSIC). La EBD se creó en 1965 como un instituto dedicado al estudio de la ecología terrestre y más tarde amplió su ámbito de conocimiento a la biología evolutiva y la ecología del comportamiento. El Instituto está constituido por su sede principal en Sevilla y dos estaciones de campo, la Reserva Biológica de Doñana y la Estación de Campo de Roblehondo (Parque Natural de las Sierras de Cazorla, Segura y las Villas). La Estación Biológica de Doñana cuenta con una sólida tradición en estudios sobre etología y ecología del comportamiento, tanto desde una perspectiva evolutiva básica como aplicada a la conservación de la fauna salvaje. Se ha Programado una visita al P. N. de Doñana el sábado día 15. Más información: Ir a la página del XIV Congreso... Descubriendo el comportamiento animal en el programa Reserva Natural, en Radio 5 26/09/2011 Descubriendo el comportamiento animal en el programa Reserva Natural, en Radio 5. Josefina Maestre ha tenido esta semana de invitado a Juan Carranza que junto Alberto Jose Redondo socio de la Asociación Española de Cine e imagen Científicos, dirigen y producen la serie “Descubriendo el Comportamiento animal” la serie que emite actualmente La 2 de TVE, de cuyos contenidos habla Juan Carranza, presidente de la Sociedad Española de Etología y uno de los responsables del proyecto. Ir a la página de Reserva Natural... Nueva emisión en La2 de TVE de la serie documental “Descubriendo el comportamiento animal” 24/08/2011 Comienza una nueva emisión en TVE de los documentales de la serie DESCUBRIENDO EL COMPORTAMIENTO ANIMAL producidos por la SEE. La emisión será a partir del próximo viernes día 26 de Agosto, a las 14:30h por La2 de TVE, de lunes a viernes. Se emitirán 21 capítulos, 12 que ya emitieron el pasado año y 9 capítulos nuevos que se han producido durante el 2010 y que no han sido emitidos hasta el momento. Disponible para descarga el libro Etología - Introducción a la Ciencia del Comportamiento, J. Carranza (1994) 08/06/2011 Está ya disponible para descarga libre en la sección de publicaciones el libro Etología. Introducción a la Ciencia del Comportamiento - Juan Carranza, Publ. Universidad de Extremadura, 1994, en formato PDF (9.6 MBytes). Ir a la página de descarga... Clausura del Máster Universitario en Etología 2010-2011 15/04/2011 Se ha clausurado el Máster en Etología por la Universidad de Córdoba. El acto estuvo presidido por la Directora del Secretariado de Másteres y Prospectiva de la UCO, Mar Delgado, la Vicedecana de Investigación, Relaciones Internacionales y Movilidad de la Facultad de Ciencias de la UCO, Mª Teresa Roldán y los directores académicos del Máster y Profesores del Departamento de Zoología, Luis Arias de Reyna y Pilar Recuerda. Los 26 alumnos que han cursado este Máster en su primera edición (véase foto más abajo), en el curso 2010-2011, recogieron un diploma acreditativo. Los estudiantes, pertenecientes a ocho comunidades autónomas, han recibido clases y conferencias de una gran cantidad de especialistas en Etología de nuestro país, en un Máster que ha sido patrocinado por la Consejería de Medio Ambiente de la Junta de Andalucía y promovido por la Sociedad Española de Etología. Leer más... Ya está disponible el DVD de la serie documental Descubiendo el comportamiento animal Se han editado en DVD los 12 capítulos de 5 minutos de la premiada serie documental Descubiendo el comportamiento animal producida por Alberto José Redondo Villa y Juan Carranza Almansa. Todo el material de la serie es original, tanto las imágenes como el grafismo, la música especialmente compuesta para la serie, el sonido ambiente, la locución, etc. Este DVD se entregó a todos los socios de la SEE participantes en el congreso que se celebró entre los días 21 y 24 de septiembre de 2010 en Ciudad Real (España), así como a todos aquellos participantes que se hicieron socios de la SEE durante el congreso. Leer más... Publicado un nuevo libro por la SEE: Estudios sobre Comportamiento Animal XXV años de la Sociedad Española de Etología Acaba de ver la luz el libro Estudios sobre comportamiento animal - XXV años de la Sociedad española de Etología patrocinado por la Universidad de Extremadura y por la SEE en conmemoración de los XXV años de la Sociedad Española de Etología Este libro recopila una serie de artículos publicados en la revista Quercus sobre comportamiento animal por varios investigadores de la Sociedad Española de Etología. Durante la celebración del XIII Congreso de Etología que se celebró del 21 al 24 de septiembre en Ciudad Real (España), se entregó un ejemplar del libro y del DVD de la serie documental Descubiendo el comportamiento animal a todos los socios de la SEE, así como a todos aquellos participantes que se hicieron socios de la misma durante el congreso. Leer más... >> Ver entradas antiguas << Contactar con la S.E.E. © Copyright 2002-2009 SEE Aviso Legal     ");
array_files[3]=new Array(0,1,"http://webs.uvigo.es/c04/webc04/etologia/publicaciones.html","2012-02-09","45K","Publicaciones de la Sociedad Española de Etología    ","",""," Publicaciones de la Sociedad Española de Etología label label label Inicio Quiénes somos Noticias Hacerse socio Publicaciones Enlaces Contactar Área privada XXV Aniversario Congreso Nacional e Iberoamericano de Etología XXIX International Ethological Conference Enseñanza de la Etología en la Universidad Vocabulario etológico Documentales Bicentenariode Darwin Concurso Fotográfico Investigación Publicaciones de la S.E.E. Las publicaciones de la S.E.E. son de dos tipos: periódicas, (revistas Etología, Acta Ethologica y EtoloGUIA) y no periódicas, como es el caso de los libros. A través de las diversas revistas periódicas, la S.E.E. abarca tanto la vertiente científica asociada a los trabajos de investigación y documentos científicos presentados en diferentes foros, como otra vertiente puramente divulgativa. Libros Revistas Libros Adaptive Behaviour: Understanding the Human Animal. Adaptación del comportamiento: comprendiendo al animal humano. Autor: Manuel Soler. La aceptación por parte de los etólogos de que el comportamiento, al igual que cualquier otra característica de los seres vivos, es el resultado de la evolución por selección natural supuso la implantación de un enfoque evolutivo que dio lugar al nacimiento de la llamada ecología del comportamiento, que se convirtió en una de las ciencias más importantes e influyentes de la biología evolutiva... ISBN: 978-84-695-2471-8 (versión en inglés) Descargar índice del libro (PDF) Descargar libro completo en inglés (PDF) Etología. Introducción a la Ciencia del Comportamiento CARRANZA, J. (Ed.) 1994. Etología. Introducción a la Ciencia del Comportamiento. Publ. Universidad de Extremadura. 590 pp. ISBN: 84-7723-173-7 Descargar libro (formato PDF, 9.6 MBytes) Fauna en acción: guía para observar comportamiento animal en España. Soler, M., Martín, J., Tocino, L., Carranza, J., Cordero, A., Moreno, J., Senar, J.C., Valdivia, M. & Bolívar, F. (Eds.) 2006. Fauna en acción: guía para observar comportamiento animal en España. Ediciones Lynx. 368 pp. ISBN: 84-96553-23. Estudios sobre Comportamiento Animal XXV años de la Sociedad Española de Etología Juan Carranza - Juan Moreno - Manuel Soler Estudios sobre Comportamiento Animal XXV años de la Sociedad Española de Etología (1984-2009) ISBN: 978-84-7723-920-8 Libro conmemorativo de los XXV años de la SEE y que recoge una serie de artículos publicados en la revista Quercus sobre comportamiento animal por investigadores de la Sociedad Española de Etología. Patrocinado por la Universidad de Extremadura y la SEE. Adaptación del comportamiento: comprendiendo al animal humano. La aceptación por parte de los etólogos de que el comportamiento, al igual que cualquier otra característica de los seres vivos, es el resultado de la evolución por selección natural supuso la implantación de un enfoque evolutivo que dio lugar al nacimiento de la llamada ecología del comportamiento, que se convirtió en una de las ciencias más importantes e influyentes de la biología evolutiva... El enfoque evolutivo de la ecología del comportamiento también se ha trasladado al estudio de los seres humanos y ha aportado un aluvión de ideas que han supuesto, en muchos casos, soluciones que han iluminado el panorama intelectual. En Adaptación del comportamiento: comprendiendo al animal humano, segundo libro de la colección promocionada por SESBE, Manuel Soler revisa los temas más importantes relacionados con el comportamiento animal y, a continuación, aplica esos conocimientos al comportamiento humano. La negativa a que el comportamiento del ser humano sea estudiado desde el punto de vista evolutivo, como el del resto de los animales, no está justificada en absoluto, puesto que somos una especie de mamífero que está incluida en el grupo de los primates. Éste, el evolutivo, es el único enfoque científico posible que puede permitir que nos comprendamos mejor a nosotros mismos. Es cierto que somos diferentes del resto de las especies, pero no porque nuestra inteligencia nos haya liberado de nuestros instintos -como han defendido habitualmente los filósofos a lo largo de la historia-, sino porque nos permite rebelarnos contra ellos. Estudios sobre Comportamiento AnimalXXV años de la Sociedad Española de Etología Page Up Revistas La SEE ha publicado la revista Etología, de carácter científico hasta 2004, y el boletín EtoloGUIA, de carácter divulgativo, que sirve de canal de comunicación entre los socios. A partir de 2005 la revista científica de la Sociedad es Acta Ethologica, publicada por Springer-Verlag. Ambas publicaciones son enviadas gratuitamente a los miembros de la Sociedad. Revista Etología Índices de la revista Etología Resúmenes de la revista Etología Números atrasados de la revista Etología Etología empezó a publicarse en el año 1989. Etología está recogida en los siguientes servicios bibliográficos: Biological Abstracts, Cab Abstracts, Cambridge Scientific Abstracts, Cindoc, Elsevier BIOBASE, E-psyche, Pascal, Wildlife Review Abstracts y Zoological Record. Editor-Jefe: Luis Arias de Reyna Martínez, Universidad de Córdoba, España. Secretario de Redacción: Juan Carlos Senar, Museu de Zoología, Barcelona, España. Editores: Juan Carranza, Universidad de Extremadura, España. Adolfo Cordero, Universidade de Vigo, España. Phillip Heeb, Universitè de Lausanne, Suiza. Juan Moreno, Museo Nacional Ciencias Naturales, CSIC, España. Comité Científico (volumen 9): Mats Björk1und, Uppsala University, Suecia Jean Clobert, Univ. Pierre et Marie Curie, Paris, Francia William G. Eberhard, Universidad de Costa Rica, Costa Rica Patricia Adair Gowaty, University of Georgia, USA Geoffrey E. Hill, Auburn University, USA Neil B. Metcalfe, Glasgow University, UK Miguel Tejedo, Estación Biológica de Doñana, CSIC, España Tore Slagsvold, University of Oslo, Noruega Marco Apollonio, Universitá di Pisa, Italia Marcelo Cassini, Universidad Nacional de Luján, Argentina Marco Festa-Bianchet, Université de Sherbrooke, Canadá Montserrat Gomendio, Museo Nacional Ciencias Naturales, CSIC, España Ruth Newberry, Pacific Agriculture Research Centre, USA Page Up La revista EtoloGUIA publica artículos de revisión y metodológicos, resúmenes de Tesis y Tesinas, informaciones sobre congresos, y otros temas de interés relacionados con la Etología. Editor-Jefe: Vittorio Baglione (Dpto. Ciencias AgroforestalesUniversidad de Valladolid, Avda. de Madrid 44, 34004 Palencia). Editores adjuntos: Sebastián Hidalgo de Trucios (Universidad de Extremadura). Juan Carlos Senar (Museu de Zoología, Barcelona). Daniela Canestrari Descargar/Download (PDF) EtoloGUÍA vol. 21 Page Up Contactar con la S.E.E. © Copyright 2002-2009 SEE Aviso Legal     ");
array_files[4]=new Array(0,1,"http://webs.uvigo.es/c04/webc04/etologia/index_old.html","2012-02-09","31K","Sociedad Española de Etología    ","",""," Sociedad Española de Etología label label label Inicio Quiénes somos Noticias Hacerse socio Publicaciones Enlaces Contactar Área privada XXV Aniversario Congreso Nacional e Iberoamericano de Etología XXIX International Ethological Conference Enseñanza de la Etología en la Universidad Vocabulario etológico Documentales Bicentenariode Darwin Concurso Fotográfico Investigación Entradas antiguas Volver a la página de inicio Máster Universitario en Etología 2010-2011 El próximo curso, 2010-2011, se comenzará a impartir en la Universidad de Córdoba, el Máster Universitario en Etología, promovido por la Sociedad Española de Etología. El Máster pretende proporcionar una formación científica avanzada que permita a los alumnos conocer el comportamiento animal e incluirlo en el contexto de las características biológicas que, fácilmente moldeables, proporcionan una base evolutiva y ecológica que permita un uso más racional de los animales... Leer más... Comienza a emitirse en TVE la serie documental “Descubriendo el comportamiento animal” El próximo lunes 26 de Abril de 2010 se iniciará la emisión en La 2 de TVE de la serie documental Descubriendo el Comportamiento Animal, producida por Alberto José Redondo Villa (Profesor del Departamento de Zoología de la Universidad de Córdoba) y Juan Carranza Almansa (Catedrático del Área de Zoología de la Universidad de Extremadura, Director de la Cátedra de Recursos Cinegéticos y Piscícolas de la Universidad de Córdoba y Presidente de la Sociedad Española de Etología). Cada capítulo será emitido en torno a las 18:40-18:45 horas, entre Grandes Documentales y El Hombre y la Tierra. Leer más... Congreso de Etología 2010 XIII Congreso Nacional y X Iberoamericano de Etología Del 21 al 24 de septiembre de 2010 se ha celebrado el XIII Congreso Nacional y X Iberoamericano de Etología organizado desde el Instituto de Investigación en Recursos Cinegéticos (IREC), en Ciudad Real (España). Leer más... FALLO DEL I CONCURSO DE FOTOGRAFÍA «COMPORTAMIENTO ANIMAL» XXVANIVERSARIODELASOCIEDADESPAÑOLADEETOLOGÍA A partir de las 55 fotografías seleccionadas como finalistas, el jurado del concurso de fotografía sobre comportamiento animal, compuesto por: Presidente: Juan Carranza Vice-presidente: Juan Moreno Secretario: Juan Carlos Senar Expertos en fotografía de naturaleza: Jerónimo Torres y Jordi Vidal F. Ha decidido otorgar los siguientes premios:... Leer más... Nuevo premio para la serie documental Descubriendo el Comportamiento Animal FALLO DEL JURADO DE LA XXII CONVOCATORIA DE LOS PRISMAS CASA DE LAS CIENCIAS A LA DIVULGACIÓN Modalidad de trabajos multimedia El Prisma de Bronce al mejor trabajo multimedia destinado a la divulgación científica, y el premio dotado con seis mil euros, fue otorgado a la serie documental titulada Descubriendo el comportamiento animal, original de Alberto José Redondo Villa y Juan Carranza Almansa, por su originalidad, capacidad de síntesis y atractivo y por la importancia que tiene la implicación de los investigadores en la divulgación científica... Leer más... Presentados a la comunidad científica los nuevos capítulos de la serie “Descubriendo el Comportamiento Animal” Los tres primeros capítulos de la serie, producida y coordinada por la Sociedad Española de Etología, obtuvieron en 2008 el premio del ÁREA INVESTIGACIÓN en el XXV Certamen Unicaja de Cine, Bienal Internacional de Cine Científico. Leer más... Acta Ethologica, la nueva revista de la S.E.E. The new Journal of SEE. Índice de impacto (Impact Factor): 0.667 (2007) Acta Ethologica es la revista oficial de la Sociedad Española de Etología, substituyendo a la anterior publicación Etología. Acta Ethologica se publica conjuntamente con la Sociedad Portuguesa de Etología y el Instituto Superior de Psicología Aplicada. Acta Ethologica enfatiza estudios integrativos donde se analicen tanto los mecanismos como la función y evolución del comportamiento. Aspectos de especial interés incluyen la plasticidad adaptativa del comportamiento, variaciones inter-individuales y geográficas del comportamiento, y los procesos evolutivos que regulan el comportamiento y sus funciones. Acta Ethologica publishes empirical and theoretical research papers, short communications, commentaries, reviews and book reviews in the field of ethology and related disciplines, with a strong concentration on behavioral biology. The journal places special emphasis on studies integrating proximate (mechanisms, development) and ultimate (function, evolution) levels in the analysis of behavior. Aspects of particular interest include: adaptive plasticity of behavior, inter-individual and geographic variations in behavior, mechanisms underlying behavior, evolutionary processes and functions of behavior, and many other topics. Nota para los socios de la SEE: muchos de los contactos desde la SEE se realizan actualmente por correo electrónico. Sin embargo, se devuelven numerosos mensajes, sin duda porque las direcciones de correo-e cambian muy a menudo. Por favor, contacta con la sede si has cambiado recientemente tu dirección. Volver a la página de inicio Contactar con la S.E.E. © Copyright 2002-2009 SEE Aviso Legal     ");
array_files[5]=new Array(0,4,"http://webs.uvigo.es/c04/webc04/etologia/pdfs/Adaptive_Behaviour_-_Understanding_the_Human_Animal_-_Manuel%20Soler.pdf","2012-02-09","1556K","Adaptive_Behaviour_-_Understanding_the_Human_Animal_-_Manuel%20Soler.pdf    ","","","Adaptive Behaviour: Understanding the Human Animal Manuel Soler Copyright © 2011 by Manuel Soler ISBN: 978-84-695-2471-8 First published in 2009 in Spanish by Editorial Síntesis Original title: Adaptación del comportamiento: comprendiendo al animal humano To my parents, Dolores Cruz Ruiz and Manuel Soler Serrano. CONTENTS Forward Preface Chapter 1. Should human behavior be studied from a biological perspective? 1.1. Introduction 1.2. The uniqueness of human nature 1.3. The nature-nurture debate 1.4. Historical problems: the `naturalistic fallacy and `social Darwinism 1.5. Another controversial matter: the differences between men and women 1.6. Conclusions Chapter 2. The scientific method, natural selection and other fundamental matters 2.1. Introduction 2.2. The scientific method 2.3. Biological evolution 2.4. Natural selection 2.4.1. Natural selection in modern human societies 2.5. Adaptation 2.6. The adaptationist method 2.7. Evolutionary theory: its importance and some errors of interpretation Chapter 3. The science of ethology 3.1. Introduction 3.2. Ethology: a brief historical overview 3.3. Behavior is heritable 3.4. The objectives of ethology. Tinbergens four questions 3.4.1. The causal approach 3.4.2. The ontogenetical or developmental approach 3.4.3. The evolutionary approach (phylogenetical or historical) 3.4.4. The functional or adaptive approach 3.5. Applied ethology 3.5.1. Animal wellbeing 3.5.2. Conservation 3.5.3. Human societies Chapter 4. Reproduction, finding a mate and sexual selection 4.1. Introduction 4.2. Reproductive methods 4.3. Why does sexual reproduction exist? 4.4. What is the main difference between males and females? 4.5. Seeking a mate 4.6. Sexual selection: competition between males and mate-selection by females 4.6.1. Competition for females among males 4.6.1.1. Competition between human males 4.6.2. Male selection by females 4.6.2.1 What is it about males that females select? 4.6.2.2. How do females choose good genes? 4.6.2.3. It is not always the males who compete and the females who choose 4.6.3. Mate selection in humans 4.6.3.1 What do women and men choose when looking for a permanent partner? 4.6.3.2 Casual sexual relationships 4.6.3.3 Human secondary sexual characteristics 4.6.3.4 Sexual selection in modern industrialised societies 4.7. Male-female conflict when seeking a partner Chapter 5. Sex, fertilization, sperm competition and sexual selection by cryptic female choice 5.1. Introduction 5.2. Sexual behavior 5.3. Copulation 5.4. Sex and copulation in humans: male and female orgasms 5.4.1. Why does sexual desire happen? 5.4.2. Why do we enjoy sex? 5.4.3. What do the male and female orgasms signify? 5.5. Male-female conflict in sexual relations 5.6. Male and female genitalia 5.7. Sperm competition 5.7.1. Preventing the female from copulating with another male 5.7.2. Preventing sperm previously inoculated by other males from fertilizing the eggs 5.7.3. Taking advantage of work done previously by other males 5.7.4. Human sperm competition 5.8. Sexual selection by cryptic female choice 5.9. Fertilization without courtship: alternative strategies Chapter 6. Parental care and mating systems 6.1. Introduction 6.2. Parental care 6.2.1. Evolution of parental care 6.2.2. Parental care by males: the importance of paternity certainty 6.2.3. Which sex provides parental care? The conflict between males and females 6.2.4. Parent-offspring conflict and sibling conflict 6.2.5. Human parental care 6.3. Mating systems 6.3.1. Mating system conflict between males and females 6.3.2. Monogamy 6.3.3. Polygyny 6.3.4. Polyandry 6.3.5. Polygynandry and promiscuity 6.3.7. Human mating systems Chapter 7. Gregariousness, groups and societies 7.1. Introduction 7.2. The costs and benefits of living in a group 7.3. Adaptations to living in a group 7.4. Group structure: there are not always dominants and subordinates 7.5. How are group decisions made? 7.5.1. Consensual decisions 7.6. Coalitions alliances and superalliances 7.7. How are conflicts avoided and resolved? 7.8. Human societies 7.8.1. Despotism or egalitarianism? 7.8.2. How do human societies function? 7.8.3. The social intelligence hypothesis Chapter 8. Altruistic behavior 8.1. Introduction 8.2. How may the existence of altruism be explained? 8.2.1. Kin selection 8.2.2. Reciprocity: general features and direct reciprocity 8.2.3. Group selection 8.3. The importance of social punishment in the evolution of altruistic behavior 8.4. Altruism in eusocial insects 8.4.1. Evolution of eusociality 8.4.2. Conflict in eusocial insects 8.5. Human altruism 8.5.1. The application of general models to human altruism 8.5.2. Differentiating characteristics of human altruism 8.5.3. Factors that favor human altruistic behavior 8.5.4. Reinforced reciprocity 8.5.5. Group selection in humans 8.5.6. Is human behavior genuinely altruistic? Chapter 9. Interspecific relationships 9.1. Introduction 9.2. The relationship between a plant and its principal pollinator: coevolution 9.3. The origin and evolution of interspecific interactions 9.4. Mutualism 9.5. Commensalism 9.6. Antagonism 9.6.1. Parasitism Chapter 10. Animal communication and human language 10.1. Introduction 10.2. What is meant by communication? 10.3. Signal types in relation to the dominant senses 10.4. Signal transmission and environmental conditions: acoustic signals in birds and mammals 10.5. The cost of signals 10.6. The origin and evolution of signals 10.7. The conflict of interests between actors and receivers: an arms race 10.8. Honest communication and deceptive communication 10.9. Complex communication in animals 10.10. Human language 10.10.1. Is there anything resembling human language among other animals? 10.10.2. The origin and evolution of human language 10.10.3. Might some animals possess a poorly developed language? Chapter 11. The animal mind 11.1. Introduction 11.2. Cognition 11.2.1. The capacity for solving new problems 11.2.2. The capacity for future planning 11.3. Making and using tools 11.4. Culture 11.5. Consciousness and self-awareness 11.6. Awareness of shared consciousness 11.7. Emotions 11.8. The sense of justice 11.9. Morality and religion References 5 FOREWORD According to a Gallup poll taken in 2009 on the birthday of Charles Darwin, fewer than 40 percent of my fellow Americans accept the reality of evolution. The situation in Spain is somewhat similar, although here slightly more than 60 percent of the population believes in evolution. Of course, this means that more than 30 percent of all Spaniards do not think that evolution by natural selection has occurred, and even this is a discouraging figure. Moreover, many of those in Spain and the United States who say that they believe in evolution do not really have a sufficient understanding of Darwinian theory, much less an appreciation of the way in which modern biologists use the theory to conduct their research. Manolo Soler has recognized this reality, a point that led him to write this magnificent book to help members of the general public to advance their comprehension of a scientific concept of great importance. Dr. Soler is perfectly suited to undertake this task because he has utilized Darwinian theory as a foundation for his elegant studies of animal behavior. He is part of a group of Spanish ornithologists who have experienced great success in their investigations of the adaptive value of bird behavior. As a result, Dr. Soler has the necessary background with which to explain the value of evolutionary theory for scientific research. As Dr. Soler explains, Darwinian theory has two components. One part is the theory of natural selection, which helps provide a way for biologists to identify the adaptive value or function of the characteristics of living things that interest them. By function, we scientists know, thanks to Darwin, that we are talking about the role the trait plays in enabling individuals to reproduce successfully. The first part of this book provides an accessible account of this point with many examples drawn from fascinating recent studies conducted by biologists in Spain, Europe and the United States of America. All of these top researchers have made important discoveries that were dependent upon an understanding of natural selection theory. This theory guides the investigator when he or she is trying to develop hypotheses (explanations) for some intriguing aspect of the natural world. A wonderful example of science in action that you will encounter in this book involves the behavior of the black wheatear, whose males carry many rocks to places where their mates will build their nests. Why do the males behave this way? The first step toward a solution is to develop one or several hypotheses on the possible reproductive benefit of this characteristic. Manolo Soler and his colleagues have developed several such ideas based on a Darwinian foundation. They have then evaluated each possible adaptive function of this strange behavior using each hypothesis to produce testable predictions. The research team has subsequently hunted for the evidence for or against the predictions they have in hand and in this manner, they reached the conclusion that the males were demonstrating their physical condition (a trait related to their capacity to bring food eventually to their nestlings). The females use the information they receive about male parental quality to adjust their reproductive investment in eggs. Thus the rock-carrying males benefit by getting more eggs to fertilize if they can demonstrate that they are able to fully provision their youngsters when these hatch from the eggs in a nest. Without an evolutionary foundation, the biologists involved and the rest of us would have not understood why male black wheatears behave the way they do. The same applies to many other puzzles explored in the pages of this book. Why do so many animals reproduce sexually instead of asexually? Why are the eggs of any number of bird species bright blue? Why do females and males of many species that appear to be monogamous actually mate on the side with their neighbors? Why are altruistic acts extremely rare in the natural world? Manolo Soler presents the most recent scientific answers to these questions and many more. The author also demonstrates the utility, indeed the necessity, of an evolutionary focus if we are going to really understand the behavior of human beings. In the last few decades, some biologists and psychologists have made tremendous progress in applying Darwinian theory to key elements of human behavior. In this book, you will encounter a clear and convincing summary of this work. After having read the evidence, I believe that you will conclude that we can learn much about the adaptive value of our actions if we accept the possibility that we, like the black wheatear and all other animal species, have evolved under the influence of natural selection. There is another component to Darwinian theory and this element deals with descent with modification. Darwin knew that there is a long history behind each and every aspect of living things. We need to take this history into account if we wish to construct a complete picture of the behavior of all animals, including Homo sapiens. We can gain a part of this picture if we realize that 6 the adaptive characteristics of living things have changed little by little over time from a distant starting point. According to Darwin and his fellow evolutionists, each modern species has ancestors that are now extinct. Some of these ancestral species gave rise to a cluster of descendent species alive today and in these cases, we can predict that these organisms will exhibit similar attributes as a result of having inherited them from a common ancestor no long with us. The last chapters of this book present the results of comparative studies of closely species, studies done to reconstruct the history of complex traits in various animals, including our own species. Just as Darwin and others have predicted, animals derived from a common ancestor sometimes have maintained elements exhibited by this ancient species. In certain primate species closely related to us we can see traces of the species that preceded us and that endowed us with certain key attributes. Thanks to this point, we can put to the test ideas about such things as the history of the capacity for language and the cognitive aptitude of our own species. Readers of this book will learn that the evolutionary theories of Darwin even today have great significance not only for persons who study birds, insects and reptiles but also for those researchers that search for answers to questions about the function and history of our own species behavior. Evolutionary biology is not a discipline of the past but a vibrant, useful and immensely productive field of research today. We thank Manolo Soler for having written a comprehensive account that demonstrates the power and modernity of the ideas of Charles Darwin. John Alcock Arizona State University 7 PREFACE I took on the task of writing this book, the second in a series sponsored by the Spanish Evolutionary Biology Society (Sociedad Española de Biología Evolutiva, SESBE), early in 2008. After delivering eighteen lectures on `Ethology at Granada University, I decided the time was opportune to write a book on animal behaviour based on my approach to the subject in my classes. In these, where I try to encourage students to think and participate, I pose questions on adaptation in animal behaviour which include examples from the human species. I noticed from the start that posing questions on human behaviour led to an immediate increase in students interest and in their disposition to take part in class discussions. Nevertheless, for various and complex reasons which I consider in Chapter 1, ethology texts do not usually cover human behaviour ­ though some of them include one isolated chapter about this subject. For these reasons I decided to give the human species particular prominence in this book, which considers the principal themes of animal behaviour. Furthermore, this decision was supported by the enormous advances seen in recent years in relevant fields such as molecular biology, evolutionary psychology and neurobiology. The sequencing of the genome of various species and the impressive development of evolutionary psychology, together with the identification of numerous genes, neural circuits and hormones responsible for many behaviours, have very clearly shown that the fundamentals of human behaviour do not differ from those of other animals. Eleven themes comprise this book. After justifying in Chapter 1 the inclusion of the human species in a book on animal behaviour, Chapter 2 covers fundamentals such as the scientific method and the `theory of evolution by natural selection, which underpins the scientific study of behaviour. Chapter 3 summarises the history of ethology and gives an overview of current trends in this science. The three following chapters (4-6) deal with reproductive behaviour, following the logical sequence of the reproductive process: finding a mate, fertilisation and, in species with parental care, looking after the young in order to increase their chances of survival. Chapter 7 studies gregariousness in individuals that live in more or less permanent groups, which at times form very complex societies, as seen in social insects and in the human species. Groups and societies in all species, including our own, persist as a consequence of the benefits which individuals obtain through living together and helping each other. One form of helpful behaviour is known as altruism, the theme of Chapter 8. Chapter 9 studies the relationships between individuals of different species which, although sometimes resulting in benefits to both parties, most often serve the needs of one of them. Chapter 10 deals with the fascinating subject of animal communication leading to an analysis of the no less compelling subject of human language. Finally, Chapter 11 deals with the study of cognitive skills, dealing with topics such as problem-solving ability, planning for the future and tool use. In addition, this final chapter considers more rarefied matters such as culture, conscience, emotions, sense of justice, morality and religion. The layout of all chapters is similar. Initially I present what the science of ethology has revealed on the subject in other animals followed by its application to human beings. Often, and as I like to do during my classes to assist my students comprehension, I start with examples that illuminate the theoretical basis of an issue. With respect to the numerous studies described in the book, those which are discussed in detail have not been taken from other works but are based on original sources, often recently published novel research. All chapters are designed with a view to being entirely comprehensible without having to have read the preceding ones, allowing those who are especially interested in particular subjects to start the book where they please. With this in mind, scientific names are given the first time a species is mentioned in every chapter. Similarly, theories and scientific terms are cited in inverted commas on first mention in each chapter. Although I am aware that scientific names and bibliographical references interrupt the flow of the text I have decided to include them since they are indispensable to those readers seeking a deeper understanding of the subjects treated. I expect that readers who are less interested in the more scientific aspects will soon get used to ignoring these insertions, which always appear in parentheses. In any event, I believe that the scientific name of a species may be very useful for enquiring readers since it allows easy search for images or additional information on any example of particular interest of them. Thus, searching for the scientific name on Google and clicking on `Images may reveal impressive photographs of many of the described behaviours. Readers are, for example, invited to do an image search for the parasitic louse Cymothoa exigua that destroys the tongue of its fish host and settles in its place, or the marine racing stripe flatworms Pseudoceros bifurcus, which engage in fencing combat with their enormous erect penises, each attempting to penetrate the other. You may also wish to search for images of Pan paniscus, which will lead to video images of the frontal copulation in which bonobos indulge. Separate text boxes are used to present the most specialised theoretical knowledge. These are independent of the text and are not necessary for understanding the chapters. They need concern only those interested in acquiring more specialised knowledge. Acknowledgements This book is not just the result of having a year in which to write it but is instead the fruit of my entire professional career, during which I have been privileged to learn what so many scientists have previously discovered. I am indebted to numerous persons, institutions and, indeed, learning experiences for their assistance and for their influence on me during all this time. I will try to summarise them briefly. From a professional standpoint, and as a small tribute to Darwin in this year 2009, in which we commemorate the 200th anniversary of his birth and the 150th anniversary of the publication of his famous book 8 `On the Origin of Species, I first want to thank him, Charles Darwin, since his theory on evolution by natural selection converted biology into a true science and blazed a path for successive generations of biologists. It is no coincidence that both the first and the final references cited in this book are works by Darwin. I have enjoyed and learnt much from conversations on science with many colleagues and scientist friends, both Spanish and foreign. I would not wish to omit anyone but this paragraph would be excessively long if I were to mention them all, so I will confine myself to the two persons to whom I feel especially indebted, to the extent that I consider them my mentors who enabled my education as a evolutionary biologist: Anders Møller and Juan Moreno. I am grateful to past and present members of my research group for their readiness to collaborate and to assist with general subjects that were not always their particular priority. This willingness has helped new recruits to the group and has made my own workload lighter. I particularly want to thank my brother Juan, the first member of my group, my `helper number one as I used to call him in the days when he preferred to accompany me into the field to inspect jackdaw nests instead of attending classes at his college. It is many years now since he started working independently and he now heads his own research group (although we continue to collaborate frequently) but I want to express my enormous gratitude to him. My professional development would have been much slower without his help and collaboration. My thanks too to my ethology students, especially to those who enjoyed it, who were the majority (the course is optional and so most of those who choose to attend do so because they are interested in the material). The interest and enthusiasm which they showed during my lectures made my work more enjoyable. I was always fascinated by research work but until 1990, when I began to teach the subject etology, I never suspected that I would enjoy teaching so much. With respect to this book, many people have read some of the chapters and their suggestions have helped to improve the text. They have included biologists and professional researchers such as Vittorio Baglione, Daniela Canestrari, Juan Carranza, Laureano Castro, Adolfo Cordero, Florentino de Lope, Manuel MartinVivaldi, Santiago Merino, Jesús Mosterín, Andrés Moya, Julio Sanjuán, Juan Carlos Senar, Eduardo Tejero and Alberto Tinaut. I have also shown chapters to some friends who lack specialist biological knowledge but are interested in the various topics. Their suggestions, above all, have helped me to improve the accessibility of certain paragraphs to readers without a specialist Charles Darwin, since his theory on evolution by natural background in biology: Juan Alonso, Manuel Amezcua, Mari Carmen Arroyo, Cecilio Casado, Susana Fuentes, José Carmelo Hernández, Iluminada Jiménez, Eduardo Jiménez, Luis Muriel, David Nesbitt, José Parodi, Eva Prados, Antonio Robles, María del Mar Hernández, Francisco Sánchez and Mari Carmen Soler. I particularly wish to thank the four persons who have read the entire book: John Alcock, Juan Moreno and Juan J. Soler, whose comments improved the content, and Clara Redondo, who helped to increase its readability. With respect to this English version I am indebted to Ernest García who did good work in translating into English the original Spanish text, my friend Anders Møller who has read all the chapters providing, as usual, clever suggestions, and especially to John Alcock for encouraging me to prepare this English version and for reading once again all the book offering lot of comments and suggestions that helped improve the book considerably. From a personal standpoint, I must begin by thanking my village, Guadix, whose landscape of steep hills and gullies so fascinated me that my preferred adolescent pastime was going on excursions there with my friends. These field trips, along with my attraction to animals from my earliest days, confirmed my calling as a naturalist. Among those friends I especially am indebted to Cecilio, since, in addition to our enjoyment of rambling over the hills and gullies, we shared a great fascination with living things. I still recall his natural history encyclopedia, of four green, hardback volumes, from which we learnt so much as children. I want to thank all my friends of those now distant days of adolescence and youth, not only my walking companions but also those who did not accompany us, because together we established an atmosphere of cultural and intellectual involvement which proved most important to our development. Of course, I must also thank those most important to me, my family. My parents, to whom I have dedicated this book, and my six brothers. Above all, to Teresa Ortiz Vázquez, my wife and the mother of my three children who, until her death in 2001, always gave me her help and unconditional support. I thank my children too for their understanding and patience with a scientist father who gives much time to his work. I especially thank David, the youngest, for his (usually) successful efforts to behave himself. Eva Prados Arjona has become part of my family during the past five years. She is my friend and companion and I am enormously grateful to her for having brought me the happiness and peace necessary for writing this book and, more than anything else, for having restored to me the joy of living. 9 Chapter 1 Should human behaviour be studied from a biological perspective? 1.1. Introduction We humans have always been fascinated by the behaviour of other animals and we have had a close relationship with many animal species throughout history. Some have been our enemies, others our prey. Some have been our competitors and others, a few, our allies. Since time immemorial this close relationship has obliged us to know them well. For our ancestors, eating, as much as not being eaten, often depended on being aware of and being able to predict the behaviour of the other animals that shared their habitat. We have hated some species; others we have loved, but nearly always we have admired other animals, recognising that in some ways they are superior to ourselves. Some cultures have even idolised some animals and venerated them as gods. Sometimes we have even regarded other animals as role models and not only in antiquity because this still happens today. We just have to observe (even if only via television documentaries) the dedication and perseverance of birds caring for a nest full of chicks, the great tenderness and affection with which mammal mothers care for their young, or the courage that individuals of many species display in risking, and even losing, their lives to save those of their companions. On occasions such as these we can be overwhelmed by emotion and attribute the purest and most sublime sentiments to animals such as these. I recall not long ago a group of people who were watching a TV documentary on elephants. The story told how a group of females with some young were migrating during a time of drought and scarcity. They were crossing a desert area in an apparent attempt to reach a more foodrich region. The star of the documentary was a tiny baby elephant that was in quite a weak state. After each stop its mother and the other females helped it to get up and pushed it so that it would resume walking. When the little one died, the group stayed by the dead infant and its mother for a considerable time. Eventually, all elephants apart from the mother resumed their trek once again. The mother, although she had not eaten for a long time, remained for two days, preventing the vultures from devouring the corpse. At the end of the documentary, a lady rose from her armchair wiping away her tears and said `that was more unbearable than a weepy soap opera. The elephants behaviour revealed in the documentary was not a confection of special effects. It was real. Infancy in elephants is very lengthy and the mother and the other females, who are also related to the young, really are extremely solicitous. People who saw the documentary said such things as `they feel it more than many people do or `they are better than many people. By `better they clearly imply `better people and it is curious to hear elephants described as being better people than many real people! We humans enjoy making comparisons of this sort. One need only spend a few minutes listening to someone talking about his or her pet. Sometimes the pet owners attribute moral virtues to them, as did the watchers of the elephant programme. Often too they are regarded as possessing the highest cognitive capacities. In any event, without paying much heed to owners opinions of their pets, which tend to be very unscientific, we can ask ourselves `is human behaviour very different from that of other animals? In particular, since we have mentioned parental care, `is the behaviour of a human mother so different from that of any other type of female mammal who is caring for her young? Surely not, fundamentally. The preoccupation with her offspring, the effort to provide it with all that it needs and the readiness to take any risk to save it from danger are common to mothers of all species in which there is parental care. Why then are there no books that treat human behaviour and the behaviour of nonhuman animals similarly? That is the principal objective of this book, to tackle the study of human behaviour and that of other animals simultaneously and with the same approach. My intention, however, is not just to describe behaviours, but also to try to understand why they arise, by making use of the only theoretical framework that makes this possible: Charles Darwins `theory of evolution by natural selection (Darwin 1859). There is an important hereditary component to behaviour and it is the outcome of evolution. Evolutionary theory allows us to apply the scientific method, that is to say to suggest hypotheses and put their predictions to the test to see whether or not they are fulfilled (see Chapter 2). This is the typical scientific focus of studies of animal behaviour. Furthermore, during recent decades it has also been applied with success to the study of human behaviour as much by evolutionary psychologists as by ethologists (biologists who concern themselves with animal behaviour). I think it is important, indeed necessary, to justify from the start the validity of studying human behaviour as if we are an animal species with an evolutionary history, as this book does. Is it acceptable to study human behaviour together with that of other animals from the same biological perspective? Many philosophers, anthropologists, psychologists and sociologists would answer this question with a resounding `No for two main reasons, each in turn associated with two highly controversial matters (see Box 1.1 for a detailed explanation). Nevertheless, many biologists and also some professionals of the disciplines mentioned above would give an equally resounding `Yes to the same question. In this case the justification for their reply is simple and direct: for scientific reasons. On the one hand, we actually are animals, more specifically, a vertebrate, a mammal, a member of the order Primates. Behavioural researchers have demonstrated, without any doubt ­ as we shall be seeing throughout this book ­ that the fundamentals of human behaviour do not differ from those of all other animals. Furthermore, applying the evolutionary perspective of behavioural ecology to studies of human beings has 10 produced a flood of ideas that have led to novel insights into our behaviour. This is reflected in a large number of scientific studies that have been published during the past twenty years and that have illuminated topics such as finding a partner and falling in love, conflict between partners, the sharing (or not) of parental responsibilities, social relationships, altruistic acts and many others make more sense when seen from the viewpoint of evolutionary biology. Although such a focus remains a minority view in some disciplines, such as anthropology, it is enjoying considerable success in others, especially in psychology. Here the science of evolutionary psychology has forged ahead. It is rooted in the study of the psychological mechanisms that underlie evolution as the discipline looks to find biological similarities that are common to all human beings. Should human behaviour be studied from the same biological perspective as for all other animals? NO 1. Because many social science professionals suppose that our culture, intelligence and consciousness have liberated us from our instincts (genetic predispositions) and hence from evolutionary forces. In contrast, biology rests on the theory of evolution by natural selection, which is based on genes (see Chapter 2). Related controversial aspects a. The uniqueness of human nature (which makes us different from other animals). b. The nature­nurture debate (is human behaviour determined by genes or by the environment?). 2. Because many people believe that such a viewpoint implies justifying reprehensible behaviour. For example, they think that if violence is genetically determined, even if only partly, then murder is justifiable because it is something natural. Related controversial aspects a. The naturalistic fallacy: Assumes that what is natural is good and hence is morally acceptable. b. Social Darwinism: Proposes applying to human societies the idea that those who have triumphed are the `most fit and hence that the `less fit should not be helped to overcome their situation. YES For scientific motives exclusively: a. Because we are animals (vertebrates and mammals of the order Primates). b. Because applying evolutionary methodology has generated significant advances in our understanding of ourselves. Box 1.1. Possible replies, with their corresponding arguments and associated controversial aspects, to the question of the validity of studying human behaviour alongside that of all other animals. We shall now examine in detail the three arguments that are used to justify a negative response: the uniqueness of human nature, the nature­nurture debate and two historical problems, namely the naturalistic fallacy and social Darwinism. 1.2. The uniqueness of human nature We humans have always liked the notion that we are different from other animals. Most philosophers across history have defended the idea that although other animals have instincts human beings do not. Such an opinion insists upon the uniqueness of human nature. It maintains that each and every animal species has its own characteristic nature, all except the human species that is not subject to the dictates of genes and instincts, but rather disposes of complete liberty to forge its own nature. It is unsurprising that this idea appeals since it implies that we are superior to all other animals, which gratifies our egos and offer us the hope of free will. But can we still insist upon the uniqueness of human nature given what we now know? We are certainly different in some ways from other animals, including our closest relatives, the other primates. The chief difference, biologically-speaking, is our relatively large brain, three times larger than that of another primate of equivalent size, which implies a large increase in the number of neurons and neural interconnections. However, although we may not like to be reminded of this very much, there are many important similarities between ourselves and other animals. We are clearly mammals and share a great many mammalian characteristics. It is also apparent that we are animals that share many features with all members of the animal kingdom. For example, as in all other cellular organisms, our cells possess a genome, the gene set that instructs the development and function of each one of us. It has always been clear that if it were possible to analyse and compare the genomes of different species, including our own, this would be the key to determining the genetic differences between human beings and other animals. Such an idea was science fiction until just a couple of decades ago, but it has now been achieved by molecular biology, undoubtedly one of the branches of biology that has advanced the most in recent years. We now know that the human genome comprises some 3,000 million base pairs, which may be likened to the `letters of an encyclopaedic instruction book that contains the information needed for our construction. These 3,000 million letters are grouped into some 25,000 genes. This result came as a big surprise because bearing in mind that since the genome of Drosophila fruit-flies was already known to include about 13,000 genes, it had been assumed that the human genome would have at least 100,000 genes. Humans are after all far more complex than fruit flies and endowed with vastly greater cognitive capacities. Clearly, the discovery that we have `only 25,000 genes raised some doubt about the idea that we are on a higher level than all other living beings. The surprise was still greater when it was found that the human genome is almost identical (by 98.76%) with that of the chimpanzee (Pan troglodytes). Moreover, the chimpanzee genome was closer to our own than to the gorilla (Gorilla gorilla). These findings have been taken as a personal affront by some, since they show that not only are we animals but also that we are very similar indeed to our closest living relative. Nonetheless, although such similarities are the most striking feature of all this information, this is not to say that the differences are unimportant. As that brilliant communicator Matt Ridley (2004) has emphasised, the difference of about 1.5% from the chimpanzee genome is equivalent to no fewer than 45 million letters, which would amount to 75 Bible-length books filling a threemetre-long shelf. So, the difference may be much less than was expected, but is still very significant. What about human behaviour? It is curious (and contradictory I would say in passing) that although nobody denies the role of heredity in matters such as eye colour or height, many people refuse to accept that our genes influence our behaviour and mental abilities. Is human behaviour inherited and so in some extent 11 genetically determined as in other animals, or does it depend exclusively on conscious decisions based on our high mental capabilities? In answering this question we shall analyse a behaviour that is generally considered abhorrent from a moral standpoint: infanticide in which an individual kills an infant of its species whether through violence or simply through abandonment. Infanticide is very common in many animal groups, from invertebrates to mammals, via fish and birds. We can distinguish two types: infanticide committed by individuals unrelated to the victims and that carried out by the victims own parents. The former type is quite frequent in many species and has been much commented upon in the case of lions (Panthera leo). When a group of young male lions succeeds in taking over a pride, the males accompanying the females are driven away and most cubs are killed by the newcomers. Something similar is seen in many other mammals, not just among carnivores, but also in the primates and even birds. For example, in the barn swallow (Hirundo rustica) unpaired males may destroy the broods of established pairs. Also in polygynous species, those where a male may pair with several females, a female may break the eggs or kill the chicks of another female paired with her male. A well-known study of this involves a small marsh bird, the great reed warbler (Acrocephalus arundinaceus). Staffan Bensch and Dennis Hasselquist, of Lund University, Sweden, studied a population of this species for seven years, during which they obtained data from 279 nests. Females could be classified as monogamous (the sole mate of a given male), first polygynous (the first female to pair with a polygynous male) or second polygynous (a female paired with a polygynous male who had previously paired with another female). As would be expected, first polygynous females began to lay ahead of the second polygynous females. The investigators found that during the egg stage, nests of first polygynous females were three times more likely to be destroyed by predators than those of monogamous or second polygynous females (Bensch & Hasselquist 1994). Since all nests were in the same environment, except that those of first polygynous females were in territories in which other females were still nest building, the investigators suspected that it might have been the second polygynous females and not predators that were responsible for the destroyed clutches. They tested this hypothesis by putting plasticine eggs, of the same size, shape and colour as great reed warbler eggs, in the nests. The idea was to detect marks left by individuals that attacked the false eggs indeed, when they compared the beak marks on the plasticine eggs with those made by different bird species in the area, the impression matched those of the great reed warbler, confirming that the second polygynous females were the egg destroyers. This kind of infanticide can easily be explained in evolutionary terms. The behaviour has evolved because its perpetrators leave more descendants since natural selection favours those that practice infanticide over those that do not. Lionesses that lose their cubs because the males have killed them are ready to produce new cubs with the infanticidal males within a few months but they would not be ready to do so for a couple of years had the cubs not been killed. The infanticidal female warblers also benefit since they increase their reproductive success. When a female destroys a males other brood, she essentially force him to concentrate on feeding her chicks. As a result the killer will leave more descendants now that all the food obtained by the male is destined for her own chicks. The second type of infanticide, the one carried out by parents, is less easily explained. Natural selection penalises individuals that leave fewer descendants so that killing ones own offspring would seem to be an evolutionary mistake. We shall describe several examples before asking what possible benefits could arise from killing or abandoning ones own young. Infanticide by parents occurs in two types of situations. First, parents become infanticidal when they lack enough resources to raise their young. This is quite frequent among mammals where, if food suddenly runs short, a suckling female may abandon her young. Second, parents may kill their young if they are deformed, injured or seriously diseased, that is to say, when the chances that they will live to reproductive age are low. In such instances they too may be abandoned prematurely. One of the best studies of this type of infanticide is by Dieter Mahsberg, of Würzburg University, Germany, who worked on scorpions, invertebrates that are well known for their parental care. As is also true for some spiders, scorpions carry their young on their backs and protect them from any enemy or danger. A female scorpion does not lay eggs. The live-born young emerge from her body and climb on her back unaided. This is a difficult task and only strong, healthy young can manage it. After a couple of days the mother eats any young who have failed to climb onto her and from then on she devotes all her efforts to caring for the remaining, healthier individuals (Mahsberg 2001). The key question is whether those young who are incapable of making the climb are malformed or diseased. Mahsberg answered this question by collecting scorpion young, both those that had climbed on to their mothers and those that had not, and keeping them together in captivity under the same conditions. Most of those that had succeeded in climbing up developed into healthy adults but the majority of those that had failed to do so either died or grew into weak or deformed adults. Therefore, young that fail to climb on their mothers, and so are eventually devoured by them, would have had very little chance of reaching adulthood. Why has natural selection favoured this type of infanticidal behaviour? The answer is that it is not sufficient simply to have many offspring, these must be of good quality so that when they grow up they can compete with rivals successfully and reproduce in turn. Young that have been underfed during development or that are born with serious defects will not grow into healthy adults and their chances of reproducing successfully will be very low. Natural selection therefore favours infanticide in circumstances where food is scarce or the young are defective since investing in such offspring is a waste of effort and resources and may prejudice the survival of siblings and even the future reproduction of the parents. We said that the phenomenon of infanticide would allow us to draw some conclusions about the relationship between the behaviour of other animals and that of human beings. Infanticide is quite frequent in primates. Does it take place in humans? The answer is a resounding `Yes and a great deal of information reveals this. Without going into detail, I will list four of the 12 many studies described by the anthropologist Marvin Harris (1997): (1) Australian aborigines used to kill up to 50% of newborn babies; (2) during the 19th century the Chinese killed between 10% and 80% of girl babies; (3) in India, also during the 19th century and among particular castes, censuses showed men to be four times more numerous than women as a result of selective infanticide of girls; and (4) European parents also disposed of many unwanted children, chiefly abandoning them in hospices, which often amounted to killing them since between 80% and 90% of children left by their parents died before they were one year old. For example, 336,297 children were legally abandoned in France in just a single decade (1824­1833). It is certainly so that not all cases of human infanticide can be considered innate behaviour, but neither can they be regarded exclusively as the outcome of premeditated, conscious decisions. As usual (see the nature­nurture debate below) they probably involve both. Nevertheless, there is some evidence supporting that human infanticide is part of a reproductive strategy shaped by natural selection. For example, the highest percentages of infanticide in China occur in poor and unproductive regions. Here, if the first baby is a girl it was nearly always killed. This has a clear adaptive explanation. Bearing in mind that those who labour in the fields are all men, it is obvious that when resources are scarce it is important that a first child should be a boy, who can work and contribute to increasing food availability for the family. When the first child was a girl it meant another mouth to feed from the same resources obtained by her father, so that the well-being of the whole family would be reduced. Another fact that supports the finding that infanticide is at least partly the result of a reproductive strategy is the high rate of mortality suffered by children raised by their mother and a stepfather, compared with that occurring when children are raised by their two natural parents. For example, among the Aché, a tribe of hunter-gatherers in Paraguay, 43% of children raised by their stepfather die before they reach the age of 15, whereas only 19% of those who live with their fathers die (Hill & Hurtado 1996). Proportionally similar data exist for our own societies. Thus Daly & Wilson (1988) showed that child mortality was very low when children are raised by their biological parents (fewer than ten children under two years old per million). But, when one parent was replaced by a stepfather or a stepmother that mortality rose to nearly 650 children per million. However, Daly & Wilson (1988) suggested the possibility that step-father infanticide is a maladaptive side-effect of a generally psychological mechanism, namely the neural circuitry that causes people to favour their own genetic offspring and to feel far less interest in the offspring of others. Anyhow, the psychological mechanisms involved in this process that obviously require genes for their development, and thus our behavior, have been shaped by natural selection. Evidently, in the remote past, men who did not concern themselves with previous children of their mates, and allowed (or caused) these to die, left more descendants than those that did not behave in this way. The former ensured that all the pairs resources were dedicated to their joint offspring and so natural selection would favour this behaviour. There is no reason why step-parents should always by chance be `worse people than true parents, thus there is no reason to think that their neglect of their step-children should always be due exclusively to conscious decisions. Although some of the instances described above can be considered to be culturally-acquired learnt behaviour (given that cultures may reinforce conduct that benefits individuals in terms of their reproductive success; see Chapter 8), the fact that infanticide appears in a great diversity of cultures, and always in situations where resources are scarce, suggests that it may be an adaptation. Therefore, most behavioural biologists and evolutionary psychologists have concluded that it is impossible nowadays to maintain that human nature is in a category of its own and distinct from the nature of other animals. Discoveries emerging from different scientific perspectives, especially biological ones, indicate precisely the opposite. Human beings do have many species-specific characteristics, which are present in all societies and cultures, and such characteristics are the outcome of the evolutionary processes that gave rise to our species and that define and set the boundaries of human nature. As Jesús Mosterín, one of the most prestigious Spanish philosophers has said, contrary to some of his colleagues: `in our times, the only intellectually honest way of regarding the topic (of human nature) is with an evolutionary focus (Mosterín 2006). 1.3. The nature-nurture debate The famous nature­nurture debate, also known as the nature­environment or the inheritance­environment debate, is intimately related to the subject of human nature. This debate started off as a discussion between scientists and, as tends to happen in such matters, each side pushed the other to take up ever more extreme positions. The most radical geneticists maintained that all behavioural traits are genetically determined and that living things are puppets directed by their genes. Conversely, the most extreme environmentalists maintained that human beings are `blank slates, born with nothing predetermined, and that the brain is like an empty book that is gradually filled by our day-to-day experiences and it is these which forge our characters (see Pinker (2003) for a convincing argument against the blank slate idea). Such extreme ideas now receive scant support but, nevertheless, the debate continues, especially fanned by the media since journalists take advantage of any news that may generate sensationalist headlines, and, unfortunately, as a result, many people reject the idea that genes could play an important role in human behaviour, for the simple reason that if this were so instincts that could provoke morally unacceptable behaviour, such as selfishness, violence, sexism and so on, would have to be accepted since they would be inbuilt and unavoidable. This debate is pointless and scientists rarely bother with it today. Most ethologists accept that behaviour is the developmental result of a complex interaction between both genes and environment. I have no interest in taking this debate forward since not only has it proved to be one of the most sterile in the history of human knowledge, but it has also given rise to disastrous consequences when attempts have been made to apply its most extreme proposals. We have for example Pol Pot, leader of the Khmer Rouge regime that governed Cambodia between 1975 and 1979. He studied in France 13 and there accepted the notion that the human brain is a blank slate on which experience is written. On his return to his country he succeeded in taking power and set in motion a plan to create `a new society. He shut off Cambodia from all external influences and took a series of drastic measures. Among others, he forced the population to abandon the cities and he forbade the use of money, schools, religions and all manifestations of culture. His aim was to produce more obedient, cooperative and austere citizens. Between 1.5 and 3 million people died, according to different sources (nearly a third of the Cambodian population!). At the opposite extreme, the viewpoint that genes are all that matter, is linked to the eugenics movement, whose advocates wanted to improve the human race by controlling who is able to reproduce. Hence, for example, in the 1920s, government officials in USA and many European countries, starting from the basis that intelligence is heritable, began a program of sterilisation of the mentally retarded to prevent them from reproducing. Setting aside these historical aspects of the naturenurture debate, in which it is clear that there were neither winners nor losers, let us consider the current situation. Both viewpoints have received important support in recent years. On the one hand it has been demonstrated that not only does the environment have a great and direct influence on certain aspects such as intelligence, but also it may affect others that to many seemed to be principally determined by genetic inheritance. For example, a suitable environment may encourage an athletic child to take up sport or a studious child to read and practice other intellectual activities, in both cases because these will be most rewarding for them. On the other hand, studies comparing the behaviour of identical twins, who share the same genes, raised together or separately, have shown that nearly all personality traits have a significant inherited component, even such culturally-influenced ones as the degree of religiosity or political affiliation. However, it has also been revealed that personality does not derive from genetic determinism, in which there are specific genes for every aspect. For example, there is an important inheritable component to criminality, but this is not to say that murderers carry one or more genes that are responsible for their criminal behaviour. What happens is that there are personalities with a greater disposition to get into trouble with the law and such personalities are inheritable since they result from variation in how many genes interact. In other words, geneticists were correct when they asserted that genes are determinant and the environmentalists were also right in saying that the environment is decisive, but both were mistaken when they maintained that the other component was unimportant. More recently, and especially thanks to developments in molecular biology, there have been important advances which reveal that, the better we know the genome, the more susceptible genes are found to be to environmental influences. By way of an example we shall consider an interesting study of depression, a common and widespread psychological condition that is provoked by seriously stressful circumstances and may even drive some people to suicide. However, not all people respond to stressful circumstances in the same way. Some are highly sensitive, and may even be depressed by relatively minor matters, whereas others seem unaffected by even the most serious situations. Why do people respond to adversity in such different ways? In order to try and answer this question Avshalom Caspi, of Kings College London, UK, and his co-workers conducted a study that involved monitoring 1,037 children, who were evaluated every two years from birth until the age of 26 years. They analysed the relationship between the number of stressful episodes they experienced and any depression suffered during that period, taking particular account of the form of the 5-HTT gene that each individual possessed. This gene has two alternative forms, or alleles, one short (s) and the other long (l). These alleles code for the synthesis of a single protein, one that regulates levels of the neurotransmitter serotonin reaching the neurons. Without getting bogged down in details that are not essential for comprehending this study, the research demonstrated that individuals fall into three groups according to the types of 5-HTT alleles that they possess: two short alleles (ss), one of each (sl) or two long alleles (ll). Why was this gene investigated and not some other one? This was because the 5-HTT gene had already been discovered to have an important role in stress resistance in rhesus macaques (Macaca mulatta). The results of the human study proved very interesting. Individuals who possessed the short allele (ss or sl) suffered more depressive episodes and suicidal thoughts the more stress they had during the course of their lives. Only 10% of those who did not suffer any stressful experiences developed depression, whereas 33% of those who experienced four or more stressful episodes became clinically depressed. In contrast, those who lacked the short allele (genotype ll) were not affected by the number of stressful episodes that they encountered and only 10%­17% of them suffered any depression, irrespective of whether or not they had had any stressful experience. What do these results mean? Clearly the short allele does not by itself cause depression ­only 33% of carriers were affected at worst. But likewise not having the short allele did not exempt people from depression since at least 10% of such individuals became depressed. What the data do show is that a person whose genome includes the short allele is much more likely to suffer depression, but only in an environment in which stressful episodes are frequent. This gene affects such responses by interacting with very many other genes, but the difference between alleles is enough to influence the outcome of such interactions. The overall conclusion from this and many other similar recent studies is that `innate does not mean `inevitable, what means that the genetic programme is flexible. There is ever more evidence that genes behave as if designed to be guided by the environment. Some genes act by activating other genes, and whether or not they do so may depend on environmental circumstances. In conclusion therefore we can say that both genes and the environment have an important part to play. We have no need to fear genes. We are not their puppets but equally neither are we inevitably subject to the whims of our environmental circumstances. 14 1.4. Historical problems: the `naturalistic fallacy and `social Darwinism. As we said earlier, a second reason that explains the traditional opposition to studying human behaviour from a biological viewpoint is the belief that this angle justifies morally unacceptable conduct. It is regrettable that such an idea is still quite widespread in some intellectual circles, notably among humanists and students of social sciences, because it is rooted in errors of interpretation of evolutionary theory that have given rise to social problems across history. These errors are known as the `naturalistic fallacy and `social Darwinism. The former maintains that what is natural is good and thus morally acceptable. Such a perspective leads to the conclusion that natural tendencies, such as personal effort, will power and the drive to overcome adversity, bring about the social advancement of the individual and human progress in general. If true, those who triumph are the fittest and, conversely, that those who are less fit should not be assisted. This is what is known as social Darwinism, an argument advanced by Herbert Spencer, a 19th century philosopher who must have possessed great powers of conviction since he succeeded in getting many of his contemporaries to accept his ideas. In reality, however, the belief that the socially triumphant are the fittest has nothing to do with Darwinism, since what is achieved by effort is not encoded in the genes and thus cannot be transmitted to descendants and be subject to evolution. It should perhaps be known as `social Spencerism, never Darwinism, since it runs contrary to Darwins theory (Moreno 2007). Evolutionary fitness means something quite different from social Darwinists meant by `fit. Natural phenomena and behaviour need not be ethically acceptable. In fact, in most cases (lethal competition, predation, parasitism and many others) the conclusion may be the opposite ­what is natural is often ethically repugnant. If infanticide is adaptive and natural, this does not mean that infanticide is morally desirable! Natural selection itself is neither morally good nor bad nor does it pursue any particular objective. Despite being mistaken, the naturalistic fallacy and social Darwinism have profoundly influenced human thinking and historically they have been used to justify the unjustifiable. The horrors caused by Hitler and Stalin are extreme and opposite examples. What is worse is that these ideas continue to be used to justify the ends of some pseudo-intellectual and social circles, including ultra-feminists, assorted progressives, some religious representatives and extreme right groups, among others. Nevertheless, as we have said, both the naturalistic fallacy and the misnamed social Darwinism are erroneous and they cannot be the basis of any valid reasoning. A further problem is that both leads people to reject evolutionary thought unnecessarily. Nobody denies that differences exist, often very considerable ones, between the males and the females in most other animal species. The difficulty is that when men and women are considered, a controversy arises that may have social repercussions, since speaking of such differences is not considered politically correct in some circles. There is a widespread and mistaken impression that to speak of such differences is to highlight male superiority, although there is no reason why that should be so. The existence of differences is not to say that men are superior to women, or women superior to men, it only means that they are not the same. The existence of important differences between men and women is so obvious that you would have to be blind not to accept it or, more to the point, resolved not to do so. Apart from the sexual organs and other external sexual characteristics that distinguish the sexes, there are many other important differences, notably the physical, psychological and hormonal ones. For example, with respect to external morphology, men are larger and more muscular as well as having distinctive patterns of hair distribution and body fat. There are also clear and significant differences in characters associated with fecundity and lifespan. Men have higher juvenile mortality and they die younger than women. Women reach puberty ahead of men. There are also genetic differences, males have two different sex chromosomes, X and Y; women have two X chromosomes. The key hormonal difference is that men have higher concentrations of testosterone in the blood whereas women have more oestrogen. These hormonal inequalities are responsible for important aspects of behaviour. Testosterone makes men more competitive, ambitious and aggressive on average than women, as well as being responsible for the generally larger size and greater muscle power of men. Also, and this is what is most controversial, important differences exist in brain anatomy and in cognitive abilities. There are many differences in brain anatomy but among the most important are that the amygdala (the region responsible for impulsive responses such as fear, anger and aggression) is more developed in men, whereas the prefrontal cortex (which controls emotions) is more developed in women. As far as cognitive abilities are concerned we shall mention only three of the most important that distinguish each sex. Males tend to do better at mathematics (although not at arithmetic), have a better sense of direction and are better at solving spatial problems than women. On the other hand, women have greater linguistic fluency, are better at tasks involving precise manipulation and do a better job than men at detecting and evaluating negative emotions (see Brizendine (2006) for a detailed account of the subject). Clearly what we have given are general tendencies, not absolute differences. For example, we have said that men are taller than women but, as we all know, there are many women who are taller than many men. The same may be said of all the characteristics that we have mentioned, but the statistical trends are clear and significant. A statistical difference cannot be denied by anecdotes and exceptions, as some seem to believe. Clearly, the idea that men and women are equal is mistaken. This is not however a case of one sex being better than the other, but simply a biological reality. Biology, like evolution, is not guided by any moral 1.5. Another controversial matter: differences between men and women the Let us conclude this chapter with another issue related to human nature, the possibility that the sexes are behaviourally different in our species. Since throughout this book we shall often refer to men and women, I think it is as well to clarify some aspects of sexual differences from the start. 15 imperative. However, the biological differences in no way justify any social discrimination. Proving that the sexes differ does not imply that one has more rights than the other. The historical discrimination to which women have been subjected is properly rejected in modern society and evolutionary biologists applaud the laws and regulations necessary to do away with sex discrimination. Social equality does not require that the sexes be the same biologically. genes. Indeed, one of the things that sets us apart from other animals ­ and I think that it is the most important difference ­ is that we are the only species that has proved capable of rebelling against the evolutionary imperative that drives individuals to produce the greatest possible number of high quality descendants. Birth rates in many developed countries are now well below replacement levels. For example in Spain the rate is 1.3 children per couple. This shows that we can confront our instincts and overcome them. Genetic predispositions favour the expression of particular behaviours, but they can never obstruct the mind to the extent that nothing can be done to counter an innate tendency. I am sure that we stand to learn a great deal about ourselves the day that we come to accept our animal nature. It will allow us to see some problems for what they are, problems of evolutionary biology. Many aspects of our societies, including violence, pair formation, caring for children, parent­child relationships, altruism and social relationships, would be easier to understand were they analyzed from an evolutionary viewpoint (see Chapter 2). This is what we shall do throughout this book and it is my hope that it will serve to open the eyes of some of my readers. 1.6. Conclusions We need to forget the sterile nature­nurture debate once while also accepting our evolved human nature. We are mammals of the order Primates and we have much in common with these our closest relatives. Naturally, we also have some peculiarities of our own that make us different. Many such have been proposed, among them language, intelligence, culture, our complex societies and so on, although most of these characteristics are present in other species, even if only in an incipient form (see Chapters 10 and 11). As we have emphasised, accepting our animal condition does not mean that we are enslaved by our 16 Chapter 2 The scientific method, natural selection and other fundamental matters 2.1. Introduction As the title indicates, this book covers the study of animal, including human, behaviour. This is the concern of several sciences and ethology is one of them (see Chapter 3). As with any other science, it employs the scientific method and requires an appropriate theoretical framework, permitting investigators to make predictions that may be tested to check their hypotheses. The theory that supplies such a framework and makes scientific advances in ethology possible is the `theory of evolution by natural selection, the very same theory that underlies all the biological sciences. Given their importance, this chapter examines these two fundamentals: the scientific method and the theoretical framework in which it is applied. Box 2.1 outlines the usual steps of the scientific method. Starting from existing knowledge, scientists propose hypotheses to explain new phenomena, draw predictions arising from these hypotheses and put them to the test, to establish whether or not they are valid. A given hypothesis may generate a variety of predictions and the more of these that are not refuted the more the hypothesis is sustained. In any case, new questions arise continually and generate new hypotheses that may complement or improve upon their predecessors. Thus, when a hypothesis is sustained in many different situations it may come to be known as a theory. It should be added, however, that some theories arose as general models that had great predictive value from the start, the `theory of universal gravity and the theory of evolution by natural selection are examples. THE SCIENTIFIC METHOD: The collection of techniques, methodologies and analyses that enables the science to advance. Phenomenon requiring explanation 2.2. The scientific method Although less evident than fire, writing and the wheel, the scientific method may be said to be one of the greatest human discoveries. It has certainly been responsible for the enormous scientific and technological advancements of recent centuries, which have enabled an incredible improvement in the standards of living of human beings, at least in the industrialized countries. Nevertheless, this is not to say that all its outcomes have been positive. I cannot avoid pointing out that it has also provided our species with machines and technologies that are highly effective in resource exploitation and in large-scale destruction, to the extent that it has given humankind enormous power, sufficient to exterminate all life on earth in the short term. Humanity is becoming aware, little by little, of the danger that our development poses for the planet. There is more and more talk of `sustainable development and yet for those in government this concept may be no more than a slogan to employ when seeking to justify continuous economic growth, which each country wishes to achieve as rapidly as possible. The notion of sustainable development is utopian, given a global economy based on irrational consumerism and ongoing economic growth. Controlling population growth is the sole measure that would allow us to continue to inhabit this planet for a long time in a truly sustainable way. The scientific method may be broadly defined as the collection of techniques, methodologies and analyses that allows puzzling phenomena to be explained, from a starting point of previous scientific knowledge. Applying the method makes scientific advances possible. This definition may seem obvious but achieving the acceptance of the scientific method has not been easy. The tendency throughout most of human history has been (and continues to be except among the educated and scientifically literate) to explain natural phenomena and to answer all sorts of questions in terms of supernatural causes, religious doctrines, traditions and malevolent powers, and the like, which are fundamentally anti-scientific. HYPOTHESIS: Proposed possible explanations for a phenomenon of interest. PREDICTIONS: Outcomes or results that must be obtained if the hypothesis is correct TESTING: Carrying out the necessary tests to see whether or not the predictions are met METHODS FOR TESTING A HYPOTHESIS - Comparison between individuals - Comparative method (at the level of species, populations, etc.) - Experimental method THE EXPERIMENTAL METHOD: Consists of manipulating the characteristic responsible for producing the behaviour (according to the initial hypothesis) without affecting anything else. This would involve the `experimental group. In addition, a `control group for which nothing is manipulated is also considered. The hypothesis is considered demonstrated if significant differences are found between the results obtained for the experimental and control groups. RECOMMENDATIONS - Hypotheses must be based exclusively on existing scientific knowledge. - Hypotheses should be based on an adequate theoretical framework and thus cannot employ supernatural causes, religious doctrines, traditions, philosophical standpoints, political ideologies etc. Box 2.1. Definition and usual stages of the scientific method, testing methods and some important recommendations. We will consider in detail a very interesting example of animal behaviour which will help us to understand the scientific method better. It involves a study of a remarkable behaviour of a passerine bird, the black wheatear (Oenanthe leucura). In this species, the pair, but mainly the male, has the curious habit of carrying stones in its beak which are then dropped usually at the base of the nest but sometimes elsewhere, even far from the nest. This activity is clearly very costly. On average a bird weighing only 40g carries 300 stones, a burden of nearly two kilogrammes! The reproductive behaviour of 17 this species was little known until recently but, nevertheless, the stone-carrying habit drew the attention of ornithologists and was described early in the 20th century. The obvious question posed by this observation is `why do black wheatears carry pebbles? They must derive some benefit from it to make the high energy cost of flying when carrying pebbles in the beak worthwhile. Five of us formed a research team to study stonecarrying by the black wheatear in Guadix district (Granada province, Spain), an area where this species is relatively abundant. We devoted the first year to gathering detailed information on the reproductive biology and stone-carrying behaviour of the wheatear, since the existing data was merely anecdotal. This initial study allowed us to establish certain relevant parameters which were important in answering our original question. The principal ones were: (1) birds carry pebbles at the start of the nest building stage, (2) pebble carrying chiefly involves the males (sex that carries approximately 87% of pebbles), (3) only some of the pebbles (about a third) are deposited at the nest base, (4) pebbles sometimes form a wall at the entrance to the nest cavity, (5) pebble size is fairly uniform by a given nest (some nests have large pebbles and some have smaller ones), (6) the number of pebbles transported is highly variable, ranging from 0 to 1,300, and finally (7) pebble carrying takes place during short periods of intensive work. Based on this information, we proposed five hypotheses to explain pebble carrying (Moreno et al. 1994), all of them based on the theory of natural selection, which we will now consider briefly. The first hypothesis (nest support) proposed that the stones are used to provide a solid nest-base. This explanation generates various predictions, principally that the number of pebbles brought would depend on how irregular the surface was on which the nest was to be built. However, neither this nor other predictions relating to this hypothesis were met, there being no relationship between pebble numbers and nest-base condition. Furthermore, nests were sometimes built in sites to which no pebbles at all were transported and sometimes the stones were carried to places where nest construction was not possible. This hypothesis is therefore probably invalid. The second hypothesis (thermoregulatory function) suggests that the pebbles could play an important part in moderating broad temperature fluctuations that could prove prejudicial during incubation. Four predictions were derived from this hypothesis but, again, none of them was met. The most important of these was that the pebbles would help to reduce the cooling rate of the nest. We tested this by an experiment using old nests. We inserted a plastic bag of warm water and a temperature sensor and recorded how long it took for the water to cool from 40ºC to 30ºC. We then removed the pebbles and repeated the measurement. The stones had no effect on cooling rates, and thus, this hypothesis too was invalid. The third hypothesis (climatic protection) proposed that the pebbles serve to protect the nest from wind and rain. The most important of the predictions generated by this hypothesis was that the stones would reduce the negative effects of adverse weather conditions both on the eggs during incubation and on the brood during its stay in the nest. This prediction was not fulfilled, nor were others based on this hypothesis, since analyses of the outcome of 167 nests for which we had complete data showed that none failed for weatherrelated reasons. The fourth hypothesis (defence from predators), which suggested that the stones would difficult predator access to the nest, also generated various predictions. The principal of these was that successful nests would have more stones than predated ones. Neither this nor the other predictions were met so this hypothesis too was rejected. The fifth and final hypothesis (sexual display) proposed that stone carrying enables a male to display to a female his good physical condition and readiness to work during the breeding period, which would lead the female to adjust her reproductive output (the number of eggs laid). Given females of similar reproductive capacity, those whose mates brought many pebbles (showing that they were strong enough to bring much food to the chicks) would lay more eggs than those paired with males that carried few stones. This hypothesis is based on the `theory of sexual selection (see Chapter 4), but it should be noted that stonecarrying is unrelated to courtship, given that it is preceded by pair-formation. This hypothesis predicts that various parameters related to reproductive success would increase as the number of stones carried by the male increased. By applying the `comparison between individuals method of testing a hypothesis (see Box 2.1) we established that several predictions were met. For example, pairs that transported more pebbles laid more eggs and raised more chicks, that is to say they proved more effective at leaving descendants, in accordance with the hypothesis. The comparison between individuals method is insufficiently rigorous to establish hypotheses. These results did not allow us to consider it demonstrated but they encouraged us to start an experimental study (see Box 2.1), a much more reliable approach. Wheatear territories hold a variable number of old nests that contain pebbles transported in earlier years. We were able to show in a previous analysis that more pebbles were carried during each breeding event in those territories that contained more `old stones. It was thus necessary to clarify the effect of those `old stones since it was possible that the best males preferred the territories with most `old pebbles, because these were better territories. We began with three distinct hypotheses: females could be evaluating male quality according to the pebbles transported, according to the quantity of `old pebbles present in the territory or by taking both these variables into account. Two experiments were designed to test these hypotheses, the first of these to determine the role of `old stones and the second to determine the effect of pebbles transported prior to a given breeding attempt (Soler et al. 1996). In the first experiment we started by manipulating the number of `old stones present in the territories before the breeding season began. All the territories were randomly divided into two groups. In the first one we took away all the `old stones from the experimental group and in the other group we left all the nests as we found them for the control group (see Box 2.1). Our prediction was that if `old stones played an important role in affecting female egg laying decisions, removing them would have a negative effect on the reproductive success of the pairs that used the experimental territories. Instead removing `old pebbles had no effect 18 on the number of stones transported or on the number of eggs laid or young raised by the various pairs. The prediction was not fulfilled and thus it may be concluded that stones from former years have no effect on breeding behaviour in the wheatears. We carried out another experiment to test the hypothesis that what is important is the transport of pebbles before each nesting attempt. All nests were randomly divided into three groups. We added as many stones as had been transported by the breeding pair to the nests of the first group. We removed half of the transported stones from the second group. We neither added nor removed stones from nests of the third group although we visited them with the same frequency as we did the others (every two days). More stones were transported in the territories from which we removed pebbles than in the other two groups, indicating that the birds tend to replace the lost stones. On the other hand, those nests to which most stones were transported also had greater breeding success, pairs at these nests raised nearly twice as many chicks as did the pairs in the other two nest groups. These results support the idea that the female black wheatear adjusts her reproductive effort according to the number of stones that the male transports in her presence, and not according to the number of stones previously accumulated in the nest cavities. This finding is further supported by the fact that on all the occasions in which we saw males carrying pebbles, not only were the females always present and attentive, but also we sometimes saw them picking up some of the pebbles that the male had brought, as if to judge the weight of the stones that he had delivered. This example clearly demonstrates the process of generating alternative hypotheses and deriving predictions, as well as some of the testing mechanisms, the steps which comprise the distinct phases of the scientific method (see Box 2.1). However, this is not the end of the matter. The scientific method continues even after a hypothesis has been sustained as new hypotheses and related predictions are proposed and put to the test. A new hypothesis arose in this manner from the wheatear study: if most pebbles are carried by males then it may be predicted that, since a larger wing area would make carrying them easier, natural selection (see below) would favour a greater wing area in males than in females. We found in an earlier investigation that males do have a wing area (taking body size into account) which is significantly greater than that of females. Moreover, we obtained another interesting result that also supported the hypothesis. We found that the greater the males wing loading (the mass supported per unit area of the wing) the fewer stones it carried to the nest. Having obtained these supportive findings by the method of comparison between individuals (Box 2.1), we began another experimental study to test the hypothesis that males have evolved a larger wing area as an adaptation for stone carrying (Møller et al. 1995). We proceeded as follows. Males were randomly assigned to either of two groups. Two feathers were cut from the wings of males in the experimental group. Males in the control group were captured and measured, as were the experimental birds, but no feathers were removed. The most evident predictions were that, since cutting feathers would increase wing loading, the experimental males would carry fewer and lighter pebbles than the control males. Both predictions were fulfilled so we accepted the hypothesis that males have evolved a larger wing area as an adaptation to pebble carrying. The experimental method ­ in conjunction with the comparative method ­ is the most powerful and reliable when it comes to testing hypotheses, but it has the problem that the individuals in the experimental group have to be manipulated, which may affect their behaviour. The problem is solved by considering another group, the control group, in which the manipulation is faked. For example, if paint is being used to change the colour of some part of the bodies of the experimental group, a control for this handling would be to paint the same part of the bodies of another group using just the solvent of the paint used, i.e. without changing their colour. If this faked manipulation affects the behaviour of the control individuals, the experiment cannot be regarded as valid. Another problem with experimental handling is that it may harm the subjects of the study, raising an ethical matter that must always be taken into account. The ethical problem particularly applies to humans, a species in which no experiments involving either bodily or mental manipulations can be performed, so that most experiments are carried out by employing photographs or images after which the subjects are asked questions that will provide the desired information. We will now examine a type of experiment with human subjects that, thanks to its ingenious construction, succeed in testing a hypothesis which could not be explored previously in any other species for ethical and experimental design reasons. Staying with the sexual selection theme on which the wheatear study was based, it is frequently the case in many species (humans included) that males and females perform more or less complex dances during courtship. A hypothesis derived from this observation is that if the dance is used in mate selection, it should convey some important information about individual quality. Since it is known that the degree of symmetry is an indicator of biological quality (known as `fluctuating asymmetry, see Chapter 4), it is possible that dancing allows the evaluation of a partners symmetry. This hypothesis had never been tested because it seemed impossible to separate the effects of the dance from the physical appearance and other morphological features of the participants, which would provide direct information on symmetry. William Brown, of Rutgers University, USA, and his collaborators found a way to test this hypothesis in a human population. It consisted of evaluating the dancing ability of different persons to see afterwards whether it was related to their fluctuating asymmetry indices. To do this they filmed numerous people while they danced under special conditions. They attached markers to 41 key body points (hands, feet, shoulders, elbows, wrists etc.) of each subject and filmed them with eight special `motion capture cameras, which only record signals from the markers. The cameras were set up to cover entirely the eight cubic metres (2x2x2m) within which the subjects had to dance. The images thus obtained resemble indistinct dancing robots, which therefore avoids transmitting any information on physical appearance, as was intended. As predicted, Browns team found a significant relationship between symmetry and dancing ability and this was greater in men than in women (Brown et al. 2005). 19 2.3. Biological evolution With the exception of those religious fundamentalists who interpret the Bible literally, nowadays nobody seriously denies that all life on earth has changed over time and that all living things are derived from a common ancestor. Biological evolution is a fact. Some 80 million years ago our planet was overrun by reptiles, large mammals did not exist (although there were many small species) nor did human beings. Now, in contrast, reptiles are relatively scarce and mammals, especially humans, abound. Nowadays series of fossil remains, very complete for some groups, are available to us. These clearly record changes over time and they always reveal a perfect relationship between the sequence of appearance and a logical process of structural development in organisms. For example, jawless vertebrates appear earlier than jawed fish, which in turn appear in the fossil record before terrestrial vertebrates. Many biological sciences, and not only the study of fossils, have provided incontrovertible evidence for evolution. This books objectives do not include presenting all the evidence in favour of evolutionary theory. However, I wish to point out that not all the evidence favouring evolution is of a historical nature. There are also robust indications that evolution is active today, even in our own daily activity. For example, as all readers are surely aware, many bacteria have become resistant to a diversity of antibiotics, posing a grave threat to public health. How has this resistance been acquired? When a genetic mutation arises in a bacterium, which allows it to resist the effect of a particular antibiotic, it will survive exposure to it and will produce many copies of itself that are also resistant. Its non-resistant companions die when we use the antibiotics so that quite soon most of the bacterial population is resistant, the non-resistant ones having died off. This is clear evidence of natural selection in action. For all intents and purposes, the data in favour of evolution are so numerous and compelling that biological evolution may now be regarded as a scientific fact, as demonstrable as the existence of the atom or the orbit of the Earth around the Sun. What is evolution? In Darwins own words it is `descent with modification and this is a good definition. To be a little more specific, it may be said to be a change in the characteristics of populations of organisms over the course of successive generations. But what changes? The reply might be that what changes are the diverse morphological characteristics or behaviours of individuals. Nevertheless, this reply would not be entirely correct because it describes only what is apparent (the phenotype) and natural selection cause evolutionary change when acting upon genetically determined characteristics, which are what are transmitted to the next generation and can bring about evolutionary change. Evolution only occurs when there is a change in the gene frequencies (the genotypes) of a population. All organisms and their characteristics are the outcome of evolutionary changes. The processes of natural selection (see below) are not the only ones that can produce evolutionary changes but they are regarded as the most important. Evolutionary theory may be applied to any biological discipline, certainly including the science of animal behaviour (Soler 2002). The methods and analyses of evolutionary science have directly helped us to increase our understanding of the world around us and indeed of ourselves. Furthermore, these methods, together with the resulting knowledge, are contributing decisively to advances in applied science in fields as diverse as the conservation of endangered species, the management of natural zones and hunting reserves, medicine, agriculture, animal husbandry and biotechnology, among others. 2.4. Natural selection How is the change that we have described above and which is the key to the evolutionary process produced? In reply to this question, Charles Darwin (1859) proposed the most celebrated of his ideas, a mechanism that he called `natural selection. This is relatively simple and easy to understand if we follow the steps proposed by Darwin himself (Box 2.2). NATURAL SELECTION: Differential reproduction by hereditary variants. It penalises the less fit and so increases the proportion in the population of variants that result in improved chances of survival or in enhanced reproductive output. 1) The individuals that comprise a population differ among themselves (variation). 2) Some of the characteristics responsible for individual variation may be transmitted from parents to offspring, i.e. they are heritable (heritability). 3) Individuals have enormous reproductive potential and each generation gives rise to many descendants that never succeed in breeding as a result of competition for limited available resources (competition). 4) Survival and reproduction are not chance events. Those individuals that possess the most favoured characteristics will survive better and leave more descendants than those which lack these features. Hence a higher proportion of the favoured characteristics will pass to the following generation. Box 2.2. Definition and summary of the mechanism of natural selection What is natural selection and how does it operate? The superb studies carried out by Peter Grant and Rosemary Grant, of Princeton University, USA, will help us to understand the process. These biologists have studied the Galapagos finches for over 30 years on the islet of Daphne Major (0.34 km2) and have obtained conclusive proof of the evolutionary effects of natural selection in those populations. There were only two finch species on the island when they began their study: the common cactus-finch (Geospiza scandens) and the medium ground-finch (G. fortis). A third species, the large ground-finch (G. magnirostris) colonised the island in 1982 and these three species remain there today. The common cactus-finch feeds on the pollen and fruits of cacti but the other two species are seed-eaters, which crush seeds in their beaks, and they are potential competitors since their diets overlap. The medium ground-finch feeds on smaller seeds but the larger individuals also take the seeds of Tribulus cistoides, which are larger and comprise the favourite food of the large ground-finch. Upon the arrival of the large groundfinch, which logically was expected to eat the largest seeds -- those of Tribulus--, the investigators predicted that an evolutionary change in the medium ground-finch would result. They supposed that there would be selection for a smaller beak in the medium ground-finch, which would reduce competition with the other species and at the same time would increase their efficiency in 20 exploiting medium-sized seeds. That is to say, the consequence of the larger-beaked invaders exploiting large seeds better than the indigenous species would be that those natives that specialised on medium-sized seeds (those with smaller beaks) would leave more descendants than those specialising on larger seeds. The investigators were able to detect the evolutionary change that they had predicted in 2004, by which time the two species had coexisted for 22 years. By then the population of the large ground-finch was sufficiently large to reduce the availability of T. cistoides seeds considerably. Both species suffered great mortality after a severe drought in 2003 and 2004, which brought about a reduction in seed availability. No significant difference was observed between the beak sizes of those large ground-finches that died and those that survived. However, there was selective mortality of those medium ground-finch individuals that had larger beaks. As the observers had predicted, this resulted in an evolutionary change in that mean beak size declined in the medium ground-finch population. It was on average 11.2mm before 2003 and 10.6mm in 2005 (Grant & Grant 2006): a 5% reduction in just two years! This is a very specific study but it can help us to understand the mechanism of natural selection that gives rise to evolutionary change, as set out in Box 2.2. The first point, the existence of variation, is fundamental to the finch study and takes the form that in each species there are individuals with small, medium-sized or large beaks. The second point, the heritability of beak size, had previously been demonstrated by Grant & Grant. They found that small-beaked individuals had smallbeaked offspring and large-beaked ones produced largebeaked offspring. These two points together indicate that there is genetic variation in beak size. This is a key finding since, as we have pointed out, evolution only occurs if genetic variation exists. The third point, the deduction that many more individuals are born than succeed in reproducing, was not investigated in these finches but it is a general finding across the animal kingdom. Numerous studies of different species have shown that up to 70% of the individuals that are born die without leaving any descendants (the percentage is much higher still in species where there is no parental care, as occurs in most fish and marine invertebrates). With respect to the fourth point, which affirms that those individuals that survive to reproduce are those possessing the most favoured characteristics, the finch study demonstrated that this was the case since the medium ground-finches which survived to reproduce were principally those with smaller beaks. Although the finch study did not collect data on subsequent breeding, to have a complete view of the more or less stable evolutionary effects of natural selection we would need to take note of the long-term consequences of the process. It is evident that largebilled medium ground-finches would leave few descendants in future years since the majority of them had died. This would mean that smaller-billed medium ground-finches would predominate in the next generation, the type which would continue to exploit medium-sized seeds, those of optimum size for their beaks. Natural selection is enormously powerful and it may give rise to important evolutionary change in a population in a short period, as we have seen with the finch study. Nevertheless, caution is needed since the evolution of characteristics by natural selection is not always adaptive in the sense of improving the effectiveness of the characters under selection. Sometimes it simply acts to conserve what is useful. Since the development of many characteristics requires time and energy, i.e. is costly, if a feature is conserved it is because it is necessary or is not costly. Otherwise it would be eliminated by natural selection. Individuals that did not waste time and energy developing unnecessary characteristics would be able to devote that time and energy to producing more descendants, which in turn would displace individuals which continued to maintain costly characteristics from which they derived no advantages. There are the numerous well known instances of cave-dwelling animals which have lost their sense of vision. Another fascinating example is provided by the giant tube worms (genus Riftia) of the undersea thermal vents. These vents comprise a very peculiar deep-sea habitat where hot sulphurous emissions provide an additional source of energy. The worms and other animals of these vents have developed special adaptations permitting them to live off these sulphurous emissions. Riftia worms that obviously evolved from ancestral species with mouths and anuses may reach two metres in length but possess neither mouths nor anuses. Instead they harbour great numbers of symbiotic bacteria that metabolise the sulphur and provide the worms with all their requirements. 2.4.1. Natural selection in modern human societies Does natural selection act upon human beings in modern industrialised societies? This is a very important and highly topical question for two reasons. Firstly, because many people maintain that the important advances in medicine have reduced mortality and have prevented natural selection from operating. Secondly, because some professionals in the field, after having carried out studies intended to check adaptive hypotheses and having reached negative or conflicting results, have suggested that in human societies, people do not behave in accordance with Darwinist predictions. With respect to the first of these, although medical advances and the decline in mortality are certainly real, they need not impede the operation of natural selection, given that this acts principally on differential reproduction, i.e. if a feature makes reproduction more effective in those individuals who possess it, and that trait is heritable, it will become more frequent in the population generation after generation. The second question is much more worrying since the criticism is based on situations in which features that should result in larger numbers of descendants, according to Darwinist theory, not only do not do so but may even have the opposite effects. We shall examine this problem further because critics of the application of natural selection to human behaviour have made much of it. A clear prediction of Darwinist theory (for reasons that we treat further in Chapter 4) is that people who possess more resources (wealth) should leave more descendants than poorer people. This prediction has been found to be met in numerous studies of existing hunter-gatherer societies, especially those which allow polygamy, and in pre-industrial societies. Nevertheless, conflicting results have been found in some modern 21 societies, i.e. in these cultures richer people have fewer offspring than poorer ones. Nevertheless, various recently published studies have identified some procedural problems in certain earlier studies and they have also found that adopting more rigorous methodology does yield the results predicted by Darwinism. Among the principal problems that have stood out are, firstly, that the analysed samples have tended to include young men in the middle of their reproductive lives. Secondly, these studies use socioeconomic status as a measure of wealth, making no distinction between richness and cultural attainment, parameters that may have contradictory effects. Thirdly, it is also necessary to consider the economic attainment of men and women separately, since these two may have opposing effects. A good example of a recent study that confirms Darwinian predictions is that by Rosemary Hopcroft, of UNCCharlotte, USA. After analysing data from a United States sample between 1989 and 2000, she found some compelling and very interesting results. On the one hand it is true that both men and women of higher educational attainment produce fewer children but, on the other, men with higher salaries not only indulge in sexual relationships more often but also leave more offspring that do those whose salaries are lower (Hopcroft 2006). Another study whose results confirm and complement the previous one was carried out by Martin Fieder and Susanne Huberc, of the University of Vienna, Austria. They worked with a Swedish population sample and found that with less marked distinctions both in levels of salaries achieved and educational attainment, when both parameters rose there was an increase in the number of offspring left by men (though the number declined in the case of women; Fieder & Huberc 2007). (See also the more comprehensive study by Nettle & Pollet 2008, described in Chapter 4). the ability of organisms to survive and to produce descendants that are efficient in their environment. The beak sizes and seed-crushing behaviour of Darwins finches which we studied above are clearly adaptations that increase individuals chances of survival, which in turn enables them to reproduce and pass on the genes for a particular beak size. The pebble-carrying behaviour of black wheatears is also an adaptation that, although it does not increase survival chances, does serve to augment the fitness of individuals that carry many stones, when it comes to leaving descendants. It is easy to imagine the process which has given rise to the adaptation in these and in many other cases. Consider the eye. A cell ­or a group of cells- that is sensitive to ambient light may be considered a rudimentary eye. Nevertheless, in comparison with individuals which lacked such an eye, an individual that had one would derive many advantages, not only in finding food but also in avoiding being eaten. Any improvement that might be produced in such an organ would bring the same advantages, so that it would be expected that individuals that inherited these improvements would leave more descendants in turn. In this way, natural selection will have benefited those individuals with more highly developed vision and, after millions of generations, will give rise to the highly efficient eyes that have evolved independently in a variety of animal groups. Then, why there exist some organisms with simple eyes? The answer to this question is that only when the benefits of improved vision exceed the costs will a fancier eye to spread through a population. Imagining the evolutionary process which has given rise to an adaptation is not always so simple. There are many existing bizarre adaptations whose evolution is a genuine enigma. A remarkable example is a parasitic crustacean (Cymothoa exigua), a fish louse that replaces the tongue of its host. It enters its victim through the gills when it is very small, attaches itself to the tongue with its three pairs of anterior legs and then destroys the principal tongue artery. The tongue gradually atrophies through lack of blood and the parasite replaces it with its own body, attaching itself to the muscles that remain of the appendage. From then on, the fish uses the parasite as if it was its own tongue and it suffers no further damage. The parasite feeds whenever the fish does so and it grows as its host grows (Álvarez & Flores 1997). It is hard to imagine the adaptive process by which the parasite became converted into a tongue. Perhaps it originally only lived in the fishes mouth and the tongue-replacement strategy emerged little by little. 2.5. Adaptation The word `adaptation has a starring role in the vocabulary of evolution. Probably everyone has an idea of what it means but, unfortunately, that idea is not always correct. Hence it is worth clarifying that, although an adaptation may arise during development, this is not true evolutionary adaptation. An example will explain this. An individual who has practised swimming from a young age for several hours a day may be capable of swimming fast and far and might be said to be adapted to swimming. Another individual who has similarly from a young age dedicated many hours to playing computer games may come to be an expert player, although he well not be a great swimmer. Improvements that are acquired through lifelong practice have no effect on the evolutionary process since they cannot be transmitted to offspring. Hence, although the word adaptation may be correctly used linguistically in the sense of becoming accustomed to new circumstances, this meaning does not correspond with the idea of evolutionary adaptation. In evolutionary terms an adaptation is not the same as `adaptability. What then is an adaptation from an evolutionary standpoint? It may be defined as any characteristic that increases the biological efficiency (fitness) of individuals that possess it and which is developed through natural selection, and thus is the result of genetic changes. Biological or Darwinian efficiency is 2.6. The adaptationist method Most of the complex features of living organisms to which a task or function may be assigned are considered to be potential adaptations and one of the principal activities of evolutionary biology has been, and is, showing what these are. This type of investigation is termed the `adaptationist method. It consists of proposing a hypothesis regarding the benefits supposedly conferred by a characteristic and then demonstrating that individuals that possess it leave more descendants than those which do not. The adaptationist method is sometimes criticised for being, on occasions, over-speculative. Caution is 22 called for and at least three considerations must be borne in mind. Firstly, an ingenious idea, however evident it may seem, proves nothing by itself but has to be tested (there are three methods of testing hypotheses: comparison between individuals, the comparative method and by experiment. See Box 2.1). Secondly, alternative hypotheses must always be considered and different possibilities need to be analysed critically. Finally, not all the characteristics of an organism need be adaptations ­some may be by-products of other adaptations-, and neither need all adaptations be perfect, they may be in the process of refinement. Another matter regarding the adaptationist method needs to be considered and is important, although relates more to the terminology than to its substance. Our language is intrinsically anthropomorphic, i.e. we tend to attribute purpose and intention to animal and even to plants. Students of animal behaviour often use phrases such as `by allowing himself to be devoured by the female, the male mantis succeeds in fertilising more eggs and thus in leaving more descendants. But this does not mean that the male has consciously evaluated its behaviour to achieve its end and that it finally has decided to allow itself to be eaten. This is simply a linguistic shortcut. Such language has the advantage that it is very useful. The correct way to describe the behaviour of the male mantis to avoid anthropomorphism might be something along the lines of: `the male mantis is devoured by the female during copulation because during the course of evolution, natural selection has favoured those males that are eaten over those that succeed in escaping, given that the former leave more descendants because they are able to copulate for longer and therefore to fertilise more eggs. In other ways, without using some anthropomorphic language, a sentence becomes a paragraph. Although a little anthropomorphism is both inevitable and useful, it is necessary to be very cautious and always to make clear to ones audience and to oneself that it is only a manner of speaking and that you are not implying that animals are making conscious decisions. Rather, there are instinctive behaviours or adaptive strategies that have been selected for because they confer advantages, because they increase survival chances or because they increase reproductive efficiency. Box 2.3 but we shall only comment briefly on the most important ones. ERRORS Natural selection acts for the good of the species. SOLUTIONS The species does not come into it. Natural selection acts mainly at the level of the individual. Natural selection is `blind. It never acts towards a particular end, let alone that of solving future problems. It only improves adaptation to the environment. Although it may well produce an increase in complexity this is not always its outcome. Adaptations are the outcome of selective processes but selection can only act on existing variation, with no ultimate aim. Organisms cannot be said to be more or less evolved. All existing species are well adapted to life on our planet. Degree of evolution should not be confused with degree of complexity. Evolutionary trees only show the phylogenetic relationships between different groups. Evolution is not a ladder with human beings at the top but rather a pattern of branches in which we occupy a particular position. It is possible to produce adaptations to prevent future conditions. Natural selection acts to produce improvements and to increase complexity. Natural selection may provide an organism with the adaptations that it needs. Vertebrates are more `evolved than invertebrates Evolutionary trees indicate levels of perfection. The human being is the most evolved species. Box 2.3. The most frequent misinterpretations of the theory of natural selection and their corrections. 2.7. Evolutionary theory: its importance and some errors of interpretation The theory of evolution brought about a great revolution in biology, thanks to its enormous range of application and predictive capacity. Prior to Darwin, the biological sciences were largely descriptive. It was the theory of evolution by natural selection (Darwin 1859) which provided an adequate theoretical framework that permitted hypotheses to be produced and predictions made that could then be tested (Box 2.1). All this converted biology into a true science. Although, as we have seen, evolution by natural selection is not an excessively complex idea, it is not easily understood and as a result misinterpretations are widespread not only within the general population or among enthusiasts of natural history but also ­ and this is more serious ­ among teachers and professionals in biology. The most frequent errors are summarised in One of the most frequent errors (which is still unfortunately widespread in many countries even among biologists) is the belief that individuals act for the good of the population or the species (what is known as `group selection, see Chapter 8). For example, there is the idea that the members of a pack of wolves or a pride of lions do not fight among themselves for the good of the species, since they would injure themselves seriously or kill each other and the species could become extinct. This has been shown to be incorrect. Natural selection favours individuals which behave in ways that maximise their reproductive success, no the groups chances of survival. Those contests involving threats and displays between males are the result of natural selection since both contenders benefit if conflicts can be resolved without serious cost to the participants (see chapter 10). Another frequent error, which occurs frequently in televised nature documentaries, is to assume that natural selection generates progress and increases complexity. It is certainly true that evolution produces improvements in efficiency which, over time, tend to increase complexity. This is logical since the earliest living things were very simple and thus any changes that evolved would tend to make species more complex. However, evolution only favours improved adaptation to the environment. Hence there are many examples of selection that acts favouring the maintenance of a characteristic (stabilising selection) and also of selection that results in a loss of complexity. For example, many parasitic species have lost the digestive systems that their ancestors possessed; snakes and cetaceans have lost 23 their limbs and birds have lost their teeth, among very many other examples. Another very similar error is to believe that the human being is the most highly evolved species. Evidently this idea is highly comforting to our egos but it is nonetheless false since evolution has not progressed as a linear ascent to reach our species but rather in the form of a tree. It is a series of branches, not a ladder. Following this introduction to the scientific method and to evolutionary theory, which underpin biology and hence also the science of animal behaviour, we are now ready to begin our study of ethology. 24 Chapter 3 The science of ethology 3.1. Introduction Behaviour is characteristic of animals and it provides them with a host of adaptive responses to their environment. In its simplest form it merely involves movement, although a lack of movement ­including resting or even sleeping- may also be regarded as behaviour. In essence, really the only time an animal is not behaving is when it is dead. There are many definitions of animal behaviour. One of the most widely accepted, although it is too simple and mechanistic, is `the response of an organism to a stimulus. It may also be said to be the assemblage of mechanisms and strategies that living beings use to resolve the problems that confront them during their life cycles. Behaviours range from very simple and predictable to highly complex and unpredictable. Animal behaviour, and thus also human behaviour, is highly varied and may be studied from a diversity of viewpoints that are the province of various sciences (see Box 3.1). Ethology (behavioural biology): Mainly concerns the behaviour of animals in their natural habitats. This field, the science that is most directly associated with animal behaviour, may also include humans as an object of study. Anthropology: Deals with the behaviour of present day human beings. The most important of its various branches are cultural anthropology, which studies human cultures that may have promoted the same lifestyle for hundreds of years, and physical anthropology, which is concerned with how humans evolved. Psychology: Aims to understand the mental processes of humans and other animals, and why they behave as they do. Chiefly, deals with the mechanisms responsible for behaviour. Studies that employ animals other than humans are usually laboratory-based instead of observed under natural conditions. Sociology: Sociologists study human societies, how humans manage to conduct social life and the cultural basis for human social behaviour. Sociobiology: Deals with animal social behaviour, analysing the causes underlying the evolution of animal societies. Has since broadened its scope to encompass an adaptationist focus on animal behaviour, which means that it now also comprises what it known as behavioural ecology. Box 3.1. Sciences whose objective is the study of animal behaviour, including that of human beings. 3.2. Ethology: a brief historical overview Human interest in animal behaviour is long standing. During the Greek classical period, Aristotle devoted two volumes of his famous work Historia animalium to the subject. Among others, he gave detailed accounts of the contests between courting wild boars, the incubatory behaviour of pigeons and the reproductive strategy of the common cuckoo (Cuculus canorus), a bird that builds no nest but instead lays eggs in the nests of small bird species, which then take on the task of raising the, for them, gigantic cuckoo chicks. However, as happened with many other sciences, the quest for knowledge then faded for many centuries. This was especially the case with the study of animal behaviour since in the 17th century, when other sciences experienced a resurgence, the influential French philosopher René Descartes, came up with a disastrous notion that succeeded in destroying any interest in the subject. Descartes maintained that animals functioned as machines and therefore that knowing the machine (its morphology) and its workings (its physiology) left nothing further worth studying. This view retarded ethology for two hundred years. It is a pity that nobody gave Descartes a dog when he was a child; had they done so perhaps he would not have come up with his unhelpful conclusion. Virtually nobody took an interest in studying animal behaviour until the 19th century, when Charles Darwin, in his famous work On the origin of species, used numerous examples of animal behaviour to advance his theory on evolution by natural selection. In particular, he proposed hypotheses to explain behavioural evolution, which led to enormous advances not only in ethology, but also in biology in general (Darwin 1859). The study of animal behaviour developed greatly in Europe during the first half of the 20th century thanks to the impetus given by Darwins work. Following studies by Whitman and Heinroth, there emerged the personalities of Konrad Lorenz, Karl von Frisch and Niko Tinbergen, who received the Nobel prize in 1973 for having essentially created a new science: ethology. That ethological school was based on studying animals under natural conditions while giving maximum importance to the analysis of instinctive behaviour, which ethologists regarded as distinct from learning. At the same time, in the United States, a school of thought emerged known as comparative psychology (also known as `conductism or `behaviourism), which was opposed to ethology and maintained that what mattered was to study the mechanisms of learning under laboratory conditions. Its leading advocates, chiefly Thorndike, Watson and, in particular, Skinner, maintained that only reflexes are innate (the `classical conditioning theory developed by Pavlov) and that all else is learned by animals based on the rewards and setbacks they receive from the environment. The dispute between both camps was very fierce at times, but gradually their differences lessened, both regarding their methodology (field or laboratory) and their theoretical frameworks. Nobody nowadays maintains that animal behaviour is composed entirely of instincts or learned behaviours; all ethologists agree that every behaviour is the outcome of a very complex interaction between genetic and environmental factors. Without a doubt, the most important revolution in ethological belief came when ethologists accepted that behaviour depends upon the expression of an organisms genes, and hence heritable and subject to natural 25 selection. This means that behaviours of individuals will have been optimised by natural selective processes to maximise their reproductive success. It is this adaptationist approach that dominates ethology today and it has given rise to the discipline known as behavioural ecology, which may be defined as the branch of ethology that studies behaviour from an evolutionary viewpoint and that maintains a close relationship with both ecology and genetics. In fact, behavioural ecology has achieved such prominence that it may be considered to be modern ethology, so giving it a distinguishing name no longer makes much sense. chick of the common cuckoo and other parasitic cuckoos. The common cuckoo does not build a nest and instead, as we have noted, the females lay an egg in a nest of another bird species, which not only incubates it but also cares for the parasitic chick. Shortly after the chick hatches it sets about lifting all the other nest contents onto its back, be they eggs or other chicks (95% of the time they are eggs since the cuckoo chick tends to hatch ahead of the eggs of the host species), and tips them one by one out of the nest. Marcel Honza, of the Czech Institute of Vertebrate Biology, and his coworkers have made a detailed study of this behaviour (Honza et al. 2007), using continuous filming at nests, and the following account is based on their work except where indicated. This egg-eviction behaviour, which may even take place in the presence of the adoptive parents without their doing anything to intervene, is responsible for the typical image of a cuckoo-parasitised nest: it contains only one chick, the cuckoo. It is important to note that such behaviour may be very costly to the cuckoo chick, not only in terms of the time and energy expended but also because it may be dangerous. The cuckoo chicks determination to do a thorough job sometimes results in it too falling from the nest (Wyllie 1981). (1) Causal What causes an animal to behave in a particular way? (2) Ontogenetical or developmental How does behaviour change as an individual grows and develops? (3) Historical or phylogenetic What is the evolutionary history of this behaviour? (4) Functional or adaptive How does this behaviour influence the chances of survival and effective reproduction by individuals? 3.3. Behaviour is heritable Before going any further it is important to have one point clear: behaviour has a genetic basis. Take, for example, the case of web-spinning spiders. Their parents will have disappeared by the time they are born yet, despite being alone, they know how to build their webs perfectly well, from scratch and without being taught. However, this is not to say that there exists a gene, or a group of genes, responsible for web building, genes only direct protein synthesis and do not cause behaviour directly. The fact that an individual may carry the gene or genes responsible for a particular behaviour means, only, that the individual possesses the hereditary information needed for the development of the behaviour, but it is not certain that it will carry the behaviour out (see Chapter 1). Two circumstances may intervene: either the environmental conditions necessary for the development of that behaviour may not arise, or one or more of the genes may not be expressed adequately. Behaviour, as we have said, is the outcome of the interaction between genes and the environment and neither of these components can be said to be the most important. Invariably, the maturity, development and experience of individuals are decisive when it comes to performing a behaviour. The development of a particular behaviour has been compared to baking a cake and this is quite a useful analogy. The outcome depends on two things: the recipe (equivalent to genetic information) and the temperature and baking time (the environmental conditions). If an ingredient (gene) is missing you get a different cake. If several are missing or one of the most important ones is absent the outcome may be disastrous. The cake may also be fit only for the bin if it stays too long or too briefly in the oven, or is baked at too high or too low a temperature. Box 3.2. Tinbergens four questions 3.4.1. The causal approach Animal behaviour is highly complex and hence demands high levels of control and coordination as well making use of a great deal of information both about external environmental conditions and about the internal state of the individual. So, when we ask, what is the physical cause of behaviour, one answer focuses on the nervous system and hormonal system, which take charge of coordinating information received and bringing about the appropriate behavioural response. The resulting behaviour is actually performed by the locomotor system, both muscular and skeletal, and a great diversity of structures that make specific behavioural patterns possible. This, in summary, is the basic machinery responsible for behaviour. The nervous system integrates and coordinates both external stimuli and internal drives and thus oversees different behavioural possibilities, giving priority to some over others. Hormones affect motivation, among other things, and may increase or reduce the chances that a particular behaviour will occur. Questions associated with the cause of a particular behaviour may be considered from a diversity of viewpoints, depending on what is of greatest interest to a researcher. Thus, for example, in the cuckoo case a neurobiologist would study the nervous system when exploring the relationship between the cause of the 3.4. The objectives of ethology: Tinbergens four questions Ethology considers all possible approaches to study how and why animals interact with each other and with the environment in which they live. Niko Tinbergen, in his classic and influential work published in 1963, considered that there are four principal factors involved in the study of behaviour: causal, developmental, evolutionary and functional or adaptive. These can be expressed in what have come to be known as Tinbergens four questions (see Box 3.2). We shall consider each of these questions about behaviour by making use of a particular example, a striking and spectacular behaviour that has often been commented upon: the egg-eviction behaviour by the 26 behaviour and its effect (how the chick receives stimuli and what changes occur in the nervous system to make the chick empty the nest of its competitors). An endocrinologist would study the hormonal changes that happen in the young cuckoo before it performs its behaviour. A cognitive psychologist would try to explain the mental processes responsible for egg-eviction. An experimental psychologist, after identifying which stimuli provoke the behaviour (detecting via the sense of touch that there is something else in the nest) would be interested in obtaining more information on the stimuli and mechanisms that result in the egg-eviction. He or she would design experiments that would establish exactly which stimuli are effective and which are not. In contrast, an ethologist might attempt to investigate such aspects as the influence of time and temperature, of the presence or otherwise of the adoptive parents, of the size of the eggs requiring expulsion (which varies according to host species) and of the depth of the nest wall that needs to be climbed. 3.4.2. The ontogenetical or developmental approach The cuckoo chick does not set about expelling its nest companions the moment it hatches. Most authors say that it only does so some hours later, but Honza et al. (2007) have found that starts even later, after 40 hours on average. All observers agree however that the difficult task of climbing the nest wall with an egg on its back is performed with considerable effectiveness from the first attempt. Moreover, once the chick begins it works obsessively, hardly pausing even to eat. If eggs or host chicks are repeatedly replaced in the nest, they are ejected time and again, the cuckoo chick continuing to work until it may even die of exhaustion. However, the drive to perform this behaviour does not persist throughout the cuckoo chicks development in the nest, but tends to disappear after seven or eight days. Several important points can be derived from the above information. The nervous and locomotor systems must be sufficiently developed to make the behaviour possible. Also the fact that the cuckoo chick can carry out the task highly effectively from its first attempt, without prior learning, implies that the behaviour is innate, that is to say it is instinctive. This is not to say that the behaviour is genetically determined in the sense of depending solely on the genes within the cuckoo. Rather, it means that the gene - environment interactions that occur during the development of the chick enable it to carry out a complex task the first time the chick responds to particular stimuli in the nest. In general, this is not always the case since behaviours often require prior learning before they can be carried out correctly. The developmental approach to behaviour gave rise to three key concepts that mark the scientific beginnings of ethology: instinct, learning and imprinting. We shall now consider these briefly. 3.4.2.1. Instinct Behaviour is heritable, as noted above. An instinctive behaviour is one that is genetically determined in a large extent and that does not require learning in order to be performed to perfection. The spiders web example above is a classic case. The egg-eviction behaviour of the cuckoo chick also clearly illustrates the nature of an innate behaviour: a very complex process is carried out impeccably from the first attempt and, furthermore, with enormous dedication. Nevertheless, although the term `instinct was highly important during the period of classical ethology, it is practically never used in modern ethology since even behaviours that have a marked genetic basis need suitable environmental conditions for them to be carried out and their performance may vary according to such conditions. 3.4.2.2. Learning Learning may be described as the modification of behaviour through experience. Very many behaviours, among them foraging for food and nest building, have been shown to increase in effectiveness through practice. All animals are capable of learning. An example that illustrates this unequivocal statement come from studies of the nematode worm Caenorhabditis elegans, a very simple organism that lacks a brain. It has been studied very thoroughly and its nervous system is known to be comprised of exactly 302 neurons, interconnected in a pattern that seldom varies. Marie Gomez, of the Central Nervous System department of the Swiss company F. Hoffmann-La Roche, and her eight coworkers, showed that these worms were nonetheless capable of learning to find food. C. elegans is able to move around guided by the temperature of its medium. It was shown that when the worms found food somewhere which was at a specific temperature, they remembered it and thereafter showed a preference for environments that were at the same temperature. If the situation was altered and food ceased to appear at that temperature and was presented at another temperature, the worms progressively forgot the first temperature and starting preferring the new one. This whole process, involving both memory and learning, is regulated by the NCS-1 gene (Gomez et al. 2001). This illustrates what we have previously pointed out, that neither genes alone nor the environment produce a behaviour. The learning process associated with specific environmental conditions is also regulated by a gene (or genes). Animals are capable of learning the most extraordinary behaviours (just see the videos of animals on You Tube), but learning requires some prior capabilities. There is a widespread myth that the learning capacity of humans is greatly superior to that of other animals but, this is not entirely true. For example, rats are better than we are at avoiding poison, carrier pigeons navigate in wide open spaces much better than we do, and few people can match the ability of bees to remember a wide range of food sources that they have only just discovered. In any event, it is important to realise that each species has evolved to learn only such behaviours as will tend to advance its reproductive chances in its environment. Natural selection does not favour individuals with excess learning capacity because the running costs of a nervous system are very high, both in terms of energy and nutrition. Rats do not learn to search for nectar nor bees to avoid poisons because such abilities do not benefit them in their environments (see Chapter 12 for a more detailed treatment of this topic). 3.4.2.3. Imprinting In those vertebrate species in which the young are cared for by their parents the general rule is that the young do 27 not immediately know to which species they belong and they must learn this during their earliest hours or days. They possess a special sensitivity during this brief period during which they tend to regard whoever or whatever they see as their parents. The mechanism by which animals `learn to what species they belong is known as `imprinting. This type of learning was studied in detail by Konrad Lorenz, who collected eggs of greylag geese (Anser anser) and kept them in an incubator. When the goslings hatched they followed him as if he were their mother. In addition, Lorenz was able to show that such imprinting could be achieved with whatever sort of object (a box, a ball and even a flashing light) the goslings first saw during a relatively brief period after hatching. He also discovered that once imprinting has occurred, and the `sensitive period has passed, it becomes irreversible. Lorenz used these findings to present imprinting as proof that what is innate predominates over what is learned. However, such reasoning proved to be neither so straightforward nor so clear. When Lorenz repeated his work with another species of waterfowl, the mallard (Anas platyrhynchos), he was surprised to find that mallard ducklings would not follow him. After much further experimentation he found that for imprinting to occur in mallard ducklings they not only have to see something that moves but also they have to hear the callnote specific to their kind. We now know that the phenomenon of imprinting is much more complex and flexible than was first thought. Studies of brood parasites, to which we referred previously in this chapter, whose young are raised by individuals of a different species, have yielded very interesting information on imprinting. For example, it has been found that not all stimuli are equally effective (those offered by the true parents are far more effective than those provided by the adoptive parents), that the sensitive period may be delayed considerably and even that re-imprinting on the correct species may occur later, even during the juvenile period. Another member of the cuckoo family, the great spotted cuckoo (Clamator glandarius), is also a brood parasite like the common cuckoo. It lays its eggs in the nests of members of the crow family, which then raise the parasitic chicks. In studies of this species by my own research group we saw that adult great spotted cuckoos sometimes visited parasitised nests and they were also seen with the juveniles once the latter had flown. We interpreted such behaviour as being a necessary mechanism enabling imprinting by young great spotted cuckoos. It appears that, contrary to the belief that brood parasites are an exception and have innate knowledge of which species they belong to, juvenile great spotted cuckoos need contact with their own kind to help them to imprint on their own species. We tested this hypothesis experimentally by placing great spotted cuckoo chicks in the nests of magpies (Pica pica) in areas where the cuckoos did not occur (chiefly in Freneusse, France), so as to avoid any contact between the young birds and adults of their own species. As we predicted, once the cuckoo nestlings fledged from the French magpie nests they behaved as did the magpies own young (remaining in the territory of the pair that raised them), instead of behaving as do cuckoo nestlings in places where they normally occur (here they form groups independent of the territories of the adoptive parents). This experiment showed that despite being brood parasites, great spotted cuckoos need to undergo imprinting in order to `learn to which species they belong (Soler & Soler 1999). 3.4.3. The evolutionary approach (phylogenetic or historical) Behaviour evolves, as does every other characteristic of living beings. Hence a key question that ethologists may ask of any behaviour is how it began and how has it changed; in other words, `what is its evolutionary history? A generalized starting point is that complex behaviours, for example the songs of modern birds, have evolved from the simpler behaviours of their ancestral species. There are two distinct ways of studying the evolutionary history of behaviour: by examining suitable fossils or by means of a comparative study of living species. The former has fairly limited application since, strictly speaking, behaviours do not fossilise; instead, on rare occasions, structures associated with behaviour may do so. For example, the origin and evolution of flight in birds has been studied by examining fossil wings and feathers of avian ancestors. The other way of deducing history, the comparative method, involves analysing a specific behaviour in living species that display it and comparing it with the behaviour of related species that do not exhibit the trait in question. Some general assumptions tend to be made; for example, that if the behaviour is very widespread then it was probably present in an ancestral species of all the current ones. On the other hand, if the behaviour is found in only one or a few species in a genus this probably means that it only evolved relatively recently. In this way it is possible to reconstruct the evolutionary history of a behaviour in a group of related species. Even ancestral states can be reconstructed from the behaviour of current species and the phylogenetic relationships. A comparative study in relation to our example of egg-eviction behaviour by cuckoo chicks would be most interesting but the problem is that we lack enough information. Most genera of the subfamily Cuculinae (parasitic cuckoos) are known to show this behaviour but it is not displayed by at least two of them (Clamator and Scythrops). Unfortunately, no reliable information is available on the situation in many of the other genera of cuckoos. 3.4.4. The functional or adaptationist approach As we have seen, the evolution of different behaviours is the result of the process of natural selection. Many behaviours thus comprise adaptations that have been selected since they provide reproductive advantages for the individuals that perform them. Thus, the adaptationist approach (see Chapter 2) is based on asking what these reproductive advantages actually are. As noted previously, there are two principal approaches to answering these questions: the experimental method and the comparative method. Both involve proposing hypotheses that are then put to the test, in the former case through suitable experiments and in the latter by means of an appropriate comparative study. Returning to the egg-eviction behaviour of the common cuckoo, the key question would be: `What advantage does the cuckoo chick get from behaving in this way? The benefit must be significant since, as we have noted, the behaviour is very costly. The benefit 28 seems obvious, by ejecting its nest companions, the cuckoo gets all the food brought by its adoptive parents and does not have to share it. This benefit may well be decisive. The host species are small in size and their capacity to bring food to the nest is limited. The parasitic chick may grow to be ten times heavier than its hosts. It also needs much more food than the hosts chicks would require. It is thus easy to imagine the scenario in which egg-eviction behaviour may have evolved. The survival of the chicks of an ancestral cuckoo species that used small-sized host species, offering limited food-provision ability, may not have been very high. As soon as there emerged a rudimentary form of a behaviour, such as egg-eviction, which resulted in the parasitic chick receiving most of the food brought by its hosts, the survival chances of chicks that displayed it would increase. Such chicks would leave more descendants than those that lacked the behaviour, so egg-eviction would rapidly spread throughout the population. Natural selection would gradually favour individuals that improved the effectiveness of this mechanism and in this way the current situation evolved so that now all common cuckoo chicks hatch capable of ejecting all their nest companions. In other words, the behaviour is now universal within the common cuckoo for a simple reason: all cuckoo chicks are descendants of cuckoos who were capable of eliminating all possible competitors when they themselves were chicks. been identified. We now also know that the basic needs of animals are more than simple physical requirements, such as water, food and a suitable temperature. It is also essential to bear their ethological needs in mind or at least to provide them with an adequate environment in which they can perform all their basic behaviours. Recent studies have made it clear that animals do not have to be able to carry out all types of behaviour, but they need to be able to perform those for which they are motivated at a particular time. 3.5.2. Conservation Until quite recently, ethology was hardly involved at all in programmes for conserving endangered species. This was because ethologists have traditionally shown little interest in taking part in such programmes and conservationists have been little concerned with ethology. The situation has changed sharply and knowledge of animal behaviour is now considered so important that conservation programmes cannot ignore it. Awareness of territoriality, foraging behaviour, mateseeking strategies and suchlike is indispensable both when designing conservation action plans and when predicting the possible effects of any measures taken. The following example illustrates the importance of keeping behaviour in mind in what is currently such an important field of knowledge as conservation biology. A group of investigators led by Isabelle Côté of the University of East Anglia, UK, were studying the conservation problems of a small European river fish of the blenny family, the river blenny (Salaria fluviatilis), with a view to proposing measures to halt the continuing decline of its populations (Côté et al. 1999). The most important problem confronting this species is habitat loss due to removal of stones and sand from rivers for use as building materials. Male blennies set up nests beneath stones and attract females to spawn there. The females lay their eggs under the stones and the males protect the eggs from predators and oxygenate them until they hatch. The investigators devised a model that simulated stone extraction, using data on stone distribution from affected (extracted) and unaffected areas. Without considering data on stone selection by males, no minimum size limit of stones was included and the conclusion of applying the model was that stone extraction had no effect. However, when the reproductive behaviour of these fish was borne in mind (males prefer to select the largest stones as nest sites) the conclusion reached by the investigators was very different. Reducing mean stone basal area from 200cm2 to 50cm2 would lead to a 47% reduction in nest density and a 75% fall in egg production. By comparing fish reproduction in extracted and non-extracted zones they found that extraction had an even more negative effect than the second, more realistic model predicted. 3.5.3. Human societies Many of the problems of human society are related to the interaction between conduct and environment or, and this amounts to the same thing, between genetics and behaviour, which are the fundamentals of behavioural ecology. It is thus to be expected that ethological methods can be employed when studying social problems and human behaviour in general (see Chapter 1). Thus, for example, the adaptationist approach has 3.5. Applied ethology To end this chapter on the science of ethology it should be emphasised that the study of animal behaviour is not only important for its contributions to knowledge but also that it has made valuable inputs to such subjects as animal welfare, neuroscience, psychology, psychiatry, resource management, environmental management and the study of human behaviour. We shall consider the application of ethology to three of the most important of these. 3.5.1. Animal welfare The concept of animal welfare has changed a great deal over recent decades. Formerly it was thought that animals were fine as long as they were neither ill nor injured. However, the drastic changes wrought by the emergence of modern systems of farming industry (such as overcrowding, confinement and social isolation) in rich countries have revealed the serious problems that may affect animals when they are kept in extremely unnatural circumstances. There have also been recent increases in biomedical investigations in which literally millions of animals, most of them mammals, are used as experimental subjects. These two developments, together with greater social concern for animal suffering, have encouraged a modification of our concept of animal welfare. It is no longer considered to refer solely to physical health but also involves an animal being able to experience a suitable environment. These new concerns led to the emergence of the science of animal welfare, whose chief aim is diagnosing the physical and mental health of animals. In order to do this, indicators of physical health and other aspects of animal welfare, based on physiological parameters that quantify stress, have been developed and behaviours associated with pain, fear or frustration have 29 given interesting results in studies of murder in human societies, and hypotheses developed in studies of infanticide in other species have been applied with considerable success to understanding the maltreatment and abuse of children (see Chapter 1). The available statistical data have been found to correspond with what has been observed in other animals. For example, male child abusers are most often the current partners of the mothers and not the genetic fathers of the children involved. In other cases the results obtained from studying the behaviour of different animal species have been applied successfully to understanding some of the problems of human societies. For example, studies of how chimpanzees and other primates engage in reconciliation after a dispute have helped in the development of new treatments and strategies aimed at reducing aggression between children in establishments, such as orphanages and schools for disruptive children, where this is a particular problem. Another example is seen in the classic works on social development in rhesus macaques in which it was shown that, given the choice, baby macaques preferred to cling to a terry cloth-covered metal doll than to an uncovered one nearby even though this mannequin offered the infant a milk bottle. Studies such as this proved to be of vital importance in advancing ideas on child development and for psychiatry in general. 30 Chapter 4 Reproduction, finding a mate and sexual selection 4.1. Introduction Human beings, and all the living organisms on Earth, are the descendants of individuals which succeeded in reproducing themselves, thus passing their genes on to succeeding generations. This means that the most effective reproductive strategies have been under the influence of natural selection since the beginning of the evolutionary process. When we speak of reproduction we immediately think of sex, of sexual reproduction, but not all organisms reproduce in the same way, other forms of leaving descendants exist. Reproduction is quite a complex process which, in one way or another, succeeds in transmitting an organisms genes to the next generation. Different species pass on their genes via a range of mechanisms (see below), sexual reproduction is the best known of these simply because it is the one we employ. From an ethological viewpoint and in a logical sequence, sexual reproduction comprises various stages: finding a mate, fertilisation and care for the young. Each of these receives a chapter in this book. Here, in addition to the different reproductive methods, we shall study mate-seeking and the evolutionary mechanism that directs the process, which is sexual selection. that almost every individual is genetically unique. There are some species in which both types of reproduction alternate, for example, the aphids (Simon et al. 2002). Mitotic parthenogenesis: Females produce diploid eggs by mitosis, which give rise to offspring genetically identical to their parent. Meiotic parthenogenesis: Females produce haploid eggs by meiosis that develop directly without needing to be fertilised by a male gamete. The offspring are nearly genetically identical to their parent. Hermaphroditism: Individuals produce male gametes with which they fertilise their own female gametes. The offspring are nearly genetically identical to their parent. Sexual hermaphroditism: Each individual produces both male and female gametes but there is no self-fertilisation: the male gametes fertilise the ova of another individual. The offspring are substantially different genetically from their parents. Sexual isogamy: Males and females produce gametes of equal size that combine to give rise to fertilised eggs in which both parents have invested equally. The offspring are substantially different genetically from their parents. Consanguineous sexual anisogamy: Males and females are related to a greater or lesser extent and produce gametes of unequal size that combine to produce fertilised eggs. Females invest much more than males, since ova are much larger than spermatozoa. The offspring are substantially different genetically from their parents, but less so than in the following method. Non-consanguineous sexual anisogamy: Males and females are unrelated, produce gametes of different sizes and have descendants that are significantly different genetically from their parents. 4.2. Reproductive methods Living beings have developed many reproductive methods in order to produce descendants, whose differences from their parents will be more or less considerable according to the method used. Box 4.1 summarises the principal methods and the genetic changes in descendants to which they give rise. The box only outlines the topic since it is incomplete. Furthermore, a species may use more than one method. For example, many plants and animals can reproduce both sexually and asexually. Different reproductive methods have evolved in different species according to their habitats and ways of life, which is to say, they may be considered as adaptations that enable effective reproduction in particular conditions. This explains why such a diversity of methods exists, something that may seem strange to us. Thus, for example, there are species in which all individuals are both male and female at the same time; others in which sex changes (individuals start as females and later change into males), and vice-versa; others in which males are virtually non-existent and even others in which there are more than two sexes. In general, all types of reproduction may be considered to come under either of two major types: asexual and sexual. The main difference is that there is no genetic exchange during production of descendants by asexual reproduction unlike sexual reproduction. Hence individuals resulting from asexual reproduction are genetically identical to their parents, whereas those produced sexually bear new and unique genotypes, such Box 4.1. Some of the most important reproductive methods, indicating their consequences for the genetic differences between parents and offspring. Haploid: cells containing half the genetic complement of a particular species. Diploid: cells containing the full genetic complement of a particular species. Mitosis: asexual cellular replication. Meiosis: cell division giving rise to haploid gametes (two successive divisions result in four haploid gametes). Female aphids, which feed by sucking plant sap, reproduce asexually in spring and summer, laying unfertilised eggs that give rise solely to daughters, which also reproduce the same way. This reproductive arrangement yields a rapid increase in numbers when conditions are favourable. The ability to produce only daughters, which in turn are capable of reproducing quickly themselves, allows a female to give rise to a much greater number of grandchildren and greatgrandchildren than would have been possible by producing both males and females through sexual reproduction. Furthermore, since such daughters are genetically identical to their mother, they share 100% of their genes with her, and not 50% as would be the case with sexual reproduction. Hence, asexual reproduction generates greater efficiency in producing descendants and in transmitting ones own genes to the next generation. Sexual reproduction lacks these two advantages and has a third important disadvantage: time and energy must be expended in finding a mate and achieving fertilisation, which is also risky since it increases the probability of attracting predators or of 31 contracting infectious diseases (see Box 4.2. for more detail). Why then does sexual reproduction exist? It clearly must confer some advantage in order to prevail despite the described costs. However, before answering this question (in the next section) we shall continue describing the aphid life-cycle, which will also give us some insight into these foreseeable advantages. The aphid reproductive system changes with the arrival of autumn, when the females lay eggs that now give rise to both sexes. These males and females pair-up and produce a new generation of eggs by sexual means. It is these eggs which overwinter and hatch early in the following spring. COSTS BENEFITS 1 2 3 The chance of transmitting gene copies to the next generation is reduced by 50%. Finding a mate requires time and energy. It gives rise to genetic variation upon which natural selection can act. New gene combinations are created, which may enable solutions to environmental problems. It permits harmful DNA mutations to be countered. or less adaptive depending on environmental conditions and on the demographic characteristics of each organisms population. Secondly, maintaining sexual reproduction is not the consequence of a single factor but rather of a number of factors, so that some hypotheses may be valid for some organisms and different hypotheses for others. Nearly all hypotheses refer to an advantage of sexual reproduction which, in theory, amounts to an important disadvantage for asexual reproducers. Nevertheless, these latter have not only not died out but also, in many cases, they enjoy considerable evolutionary success, although less than that of sexually reproducing species. Asexuality tends not to spread since asexual species rarely give rise to new species. Furthermore, it is very difficult for asexual reproduction to reappear once sexual reproduction has evolved. The definitive answer to the enigma posed by the existence of sex still seems remote and much work remains to be done on the problem. GENETIC HYPOTHESES - Müllers ratchet: Harmful mutations will accumulate inexorably where reproduction is asexual but will be eliminated, thanks to recombination, by sexual reproduction. The latter will give rise to individuals with various mutations, which may be less successful and leave fewer descendants, but it will also result in descendants free of such harmful mutations, and these will produce a greater number of descendants. - Kondrashovs hatchet: The accumulation of mutations does not have a progressive effect but instead once their number reaches a certain level they become intolerable and individuals which pass this threshold die. In sexual reproduction, the elimination of harmful mutations is more effective since recombination spreads such mutations among all descendants and those that exceed the threshold die without leaving offspring. - Accumulation of advantageous mutations hypothesis: Helpful mutations are much less frequent than harmful ones. In asexual organisms, for a helpful mutation to benefit descendants, it must arise in individuals with few harmful mutations, which is improbable. Also, for two advantageous mutations to coincide in the same asexual individual, they must have been produced in the same lineage. In contrast, in sexual organisms, thanks to genetic recombination such helpful mutations are as likely to coincide as to be separated from harmful ones. ENVIRONMENTAL HYPOTHESES - The lottery hypothesis: It is in the interest of reproducing individuals to produce variable offspring (especially when the environment is itself variable). Such variation, which is the consequence of sexual reproduction, increases the chances that some descendants may bear suitable genes to survive in the environment into which they are born. - The Red Queen hypothesis: In antagonistic systems (those in which two species are mutually inimicable, e.g. parasite-host relationships), the variation resulting from sexual reproduction favours the emergence of new defences in the attacked party and new weapons in the attacking party (see Chapter 9). Courtship and pairing increases risks of injury and predation. 4 5 6 Sexually-transmitted infections may be contracted during copulation. It provokes fierce inter-male competition. It provokes major and costly conflict between males and females. Box 4.2. The most important costs and benefits of sexual reproduction when compared with asexual reproduction. 4.3. Why does sexual reproduction exist? Contrary to what many may believe, sexual reproduction is not a relatively recent evolutionary development. Although the earliest organisms undoubtedly reproduced asexually, the appearance of descendants bearing a genome resulting from an interchange of genetic material between two or more reproducing individuals arose very early in the history of life on Earth, much earlier than the emergence of the first eukaryotic cells (those enclosing their genetic material in a nucleus). Currently, and again contrary to what many may think, sexual reproduction is not restricted to multicellular organisms but also occurs in some bacteria. Given its widespread occurrence, it is evident that sexual reproduction has been an important evolutionary success. Nevertheless, the existence of sex is one of the great paradoxes of evolutionary biology, given that it has numerous and conspicuous disadvantages whereas its advantages are fewer and less obvious (see Box 4.2). Some twenty hypotheses have been proposed to explain the benefits of sexual reproduction and these fall into two categories: genetic and environmental. The most important are defined in Box 4.3 but we shall not explore the matter too deeply since, highly important though it is from the viewpoint of evolutionary biology, it is not so relevant to the behavioural aspects which are the theme of this book. It is enough to highlight a couple of conclusions. Firstly, sexual reproduction may be more Box 4.3. The principal hypotheses explaining the evolution of sexual reproduction, one of the great enigmas of evolutionary biology. Both in this chapter, and in the two that follow, which deal with reproductive behaviour, we shall focus on sexual reproduction, which is the richer and more varied alternative regarding the behavioural strategies employed. We shall begin with its two protagonists, the two sexes: male and female. 4.4. What is the main difference between males and females? In most species, males are quite different from females in various respects (in morphology, in reproductive organs and in hormonal make-up, among other things). Every year, when we reach the topic of sexual 32 reproduction I ask my students `what is the main difference between males and females? After discussion between themselves they tend to come up with twenty or so differences but they usually fail to agree which is the most important (although from time to time some clever individual who knows the answer pipes up and stifles the debate). The following example will help us to answer the question in the manner of evolutionary biologists. The anglerfish (Lophius piscatorius) is highly esteemed for its flesh, sold as monkfish, which may be found at fishmongers all year round. It has an enormous head with large jaws and pointed teeth, lacks scales and may be a metre long. This description matches those on the fishmongers slab but it is not a complete description of the species since all those on sale are females. The males are very different, they are much smaller (by up to forty times) and they live attached to the females. When a male encounters a female it bites through on her belly, penetrates beneath the skin and takes up residence there. Little by little he degenerates until he is little more than a pair of testes. His circulatory system connects with that of the female, so that he can obtain all necessary nutrients from her bloodstream. In short, the male turns into a small lump in the female, ready to fertilise her eggs when she decides to lay them. He is a true parasite and was regarded as exactly that for a long time before it was discovered that he was the male of the species. A similar reproductive arrangement is found in the 200plus species of this family (Lophidae). The differences between males and females are seldom so exaggerated. Normally there are many similarities between them although, however similar they may be, they always differ in ways that vary from one species to another. Nevertheless, there is one difference that never varies (except in very rare examples) and this distinction applies also to most plants: the type of gamete that each sex produces. Typically females produce a limited quantity of large gametes, the eggs or ova, which contain significant amounts of nutrients for the embryo. In contrast, males produce motile spermatozoa, consisting of little more than DNA and a store of sufficient energy to move. However, since sperm are not costly to produce they are generated in astronomical quantities. This last is no exaggeration. For example, according to the most conservative estimates, human males release some 180 million sperms per ejaculation (they are produced at a rate of some twelve million per hour), whereas human females produce a fixed number of ova during their lives, some 400 of them. All this means that just 20 ejaculations release 3,600 million sperm, more than enough to impregnate all the women of reproductive age currently existing on Earth. Some simple calculations have suggested that during the course of his life a single man may produce enough sperm to impregnate all the women who have ever existed throughout history. On the other hand, it should be borne in mind that the males of our species are not especially prolific when it comes to sperm production. Far from it! Many species far outstrip us. For example, our closest relative the chimpanzee (Pan troglodytes) produces some 600 million sperm per ejaculation (and it copulates much more frequently that human males do), but it too is far from the most sperm-productive species. Male fairywrens, small Australian birds (genus Malurus) produce no fewer than 8,000 million sperm per ejaculation. But even this total is very low compared with the output of male domestic pigs, which transfer nearly half a litre of semen per copulation, containing some 750,000 million sperm! Considering these figures, it is an understatement to say that males can produce astronomical quantities of sperm. Another important distinction between the gametes is in their size, which also presents overwhelming differences. In our species, whereas an ovum is almost visible to the naked eye since it measures one tenth of a millimetre across, a spermatozoan only measures some twenty-five thousandths of a millimetre in length, despite having a very long tail. In volume terms, the ovum is a million times larger than the sperm. The difference in the sizes and numbers of gametes produced by males and females is the most important one between the two sexes, not only because it applies very generally and is seen in nearly all species but also because it determines the reproductive behaviour of both males and females and has very important implications. It means that, from the very start, females invest more than males in reproduction, to which we may add that females also invest significantly more than males in the subsequent stages of the reproductive process. This is evident in mammals but also in most other animal. Very often, the males involvement in reproduction does not extend beyond fertilising the eggs. They could be said to be parasites, not in such a literal sense as in anglerfish males but because, as a general rule, they deliver little more than their diminutive and insignificant-looking gametes. Very frequently it is the females who have to provide all the necessary resources for the development of the offspring. 4.5. Seeking a mate Sexual reproduction generally does not allow a living being to reproduce all by itself, it requires the fusion of two gametes, each donated by an individual of a different sex. Hence, males and females are obliged to engage with each other if they wish to leave descendants. Finding a suitable mate is not at all easy and the matter raises numerous questions. Among the most important of these are: is mate-finding as difficult for males as for females?, do males and females employ the same strategies?, and are the priorities the same for both sexes? As a way to introduce these questions, we will consider the case of the pied flycatcher (Ficedula hypoleuca), one of the best studied bird species. The males arrive first at the start of the breeding season. They choose and occupy territories and sing frequently to advertise their possession, actively defending their space against other males if necessary. When the females arrive they immediately begin to seek a mate by visiting a number of different territories, and hence males. When a female hears a song that attracts her she approaches the male, who escorts her while he courts her, indicating the cavity that he has chosen as a nest site and showing her around his territory. The female may choose to remain with a male or to leave and find another. Should she decide to stay the male will have succeeded in finding a mate, but he may not settle for just her. Many males try to acquire a second mate, although only 10­15% succeed. A few even obtain three females (Lundberg & Alatalo 1992). 33 Having described mate-seeking in a species whose behaviour is typical we may now address the three questions that we raised previously. Clearly, the answer to all three is `no. Males find it harder to obtain a mate than do females. They must arrive earlier, compete with other males for territories and then perform costly displays (in this case song which precludes feeding and may attract predators) until a female accepts them. Moreover, the two sexes do not use the same strategies, males must attract females and the females then choose their males. Finally, the sexes differ in their priorities: for females the priority is to find an adequate male (or territory), but males are concerned with attracting as many females as possible. very often the second is the direct consequence of the first. In many species in which the males play no part in raising the young, the female pairs with the male who succeeds in expelling any rivals. When a female African elephant (Loxodonta africana) is in heat she emits a loud trumpeting that attracts all the adult males in the vicinity. The largest and strongest male will succeed in driving away the competition and it is he who mates with the female. SEXUAL SELECTION: that which acts on characters that affect the pairing-success and the numbers of descendants produced. Intrasexual selection: competition between males for females. - It acts by favouring the ability of one sex (normally the male) to compete for matings. - Such competition may be direct (by fighting), or may be more subtle (for example defending a territory, defending resources needed by females or creating a social hierarchy). - It is responsible for the emergence and evolution of weapons used by males in fights with other males (antlers, horns, tusks, spurs etc.) - Where it is intense it often results in males evolving a larger size than females. Intersexual selection: choosing of males by females. - Acts to favour the characteristics of one sex (usually the males) that are effective in attracting individuals of the other sex (usually the females). - Promotes (chiefly among males) the emergence and evolution of adornments that tend to be exaggerated and extravagant. - Is much less evident than intrasexual selection and is much harder to explain (see Box 4.5). - Females may base their choices on several secondary sexual characteristics at once. Points to note: - Both types of selection often act simultaneously. - It is not always the males who compete and the females who choose. - Post-pairing sexual selection may also occur when some characteristic of a pair member may influence future investment by the other. 4.6. Sexual selection: competition between males and mate-selection by females Why are there such clear differences in the mate-seeking behaviour of male and female pied flycatchers? It is because the reproductive potential of males and females differs. As we have already highlighted, the general rule is that females produce only a limited number of nutrient-rich ova and, furthermore, it is they who normally care for and feed the young. In short, the number of descendants that females leave depends above all on their capacity to raise them. As a general rule, males invest little or nothing into raising their descendants (although this is not so in the pied flycatcher, where male parental investment is considerable), and, as we have also pointed out, they make enormous quantities of relatively cheaply produced sperm. The males situation is thus very different, their reproductive success depends above all on the number of females that they are able to fertilise. In addition to the males greater reproductive potential, another extremely important factor explains why males compete for mates and females choose them. The sex ratio, that is the proportion of females to males, is generally 1:1, one female per male. Clearly, if there were several females to every male then competition for mates between males would not be so intense. Darwin proposed his `theory of sexual selection to account for the showy and extravagant ornaments shown by males of many species (the `secondary sexual characteristics, which we will deal with later) since these could not be explained by his `theory of natural selection, given that many of these adornments posed survival problems. He started from the premise that males compete among themselves for females while the latter choose among the former. However, Darwin never fully understood why this was so. It is explained by the arguments that we have previously expounded, which are the basis of the theory of sexual selection. Sexual selection may be defined as the selection pressure that acts upon characteristics that are solely related to increasing success in pair and the numbers of descendants that result. The intensity of sexual selection is determined by the relative investment of either sex in the reproductive process. It is strongest in the sex that invests least in raising the offspring. The flycatcher example clearly shows how the process of sexual selection has two distinct components, competition between males (intrasexual selection) and mate choice by females (intersexual selection) (See Box 4.4). However, it must be emphasised that these two processes are not independent of each other. Indeed, Box 4.4. Definition and chief characteristics of intrasexual and intersexual selection, the two components of sexual selection. Post-pairing sexual selection may also exist (Box 4.4). Juan Moreno, of the Museo de Ciencias Naturales in Madrid, Spain, and José Luis Osorno, of the Universidad Autónoma de México, have suggested that the blue colour of her eggs may provide a signal indicating whether a female is in good physical condition, information that the male uses to adjust his parental investment in his mates offspring. This idea rests on the fact that biliverdin, the pigment responsible for blue egg colour, is a powerful antioxidant. That a female could take on the handicap (see the `handicap principle, Box 4.6) of using this costly substance to colour her eggs, instead of retaining it within her body to combat the free radicals responsible for oxidation, may indicate that she is in such good condition that she can afford to squander this valuable pigment for such a purpose. Hence, bluish eggs will indicate to the male that the eggs laid are of high quality and merit parental investment, from which it may be predicted that males paired with such females will work harder at feeding and caring for the chicks than would those paired with females who had not laid such blue eggs (Moreno & Osorno 2003). 4.6.1. Competition for females among males In general males have to compete among themselves to obtain females, although there are exceptions, including species in which the opposite applies. Such competition may take a considerable diversity of forms: from direct fighting over females to trickery and the most subtle deceptions (such as joining forces with other males in 34 order to steal the females of the most dominant individuals or even disguising themselves as females, see Chapter 5). Two of the most frequent forms of competition include the defence of resources or territories, which the females need in order to raise their offspring, and the establishment of dominance hierarchies, which typically occurs in social animals that live in groups, including many mammal species, especially the primates. Males in gregarious species habitually weigh each other up and, as an outcome of these aggressive interactions, each learns from whom they must withdraw, since direct conflict would lead to defeat, and whom they could subjugate. This gives rise to a society with a clear hierarchy in which the most dominant individuals have preferential access not only to food but also to the females. Susan Alberts of Duke University in Nairobi, Kenya, and her co-workers have shown, in a fairly recent study of a wild yellow baboon (Papio cynocephalus) population in east Africa, which not only do the higher ranking males copulate with more females but they also father most of the babies whose mothers were in heat when those males were present. When a female is in heat her genital area begins to swell and so becomes very visible to all males in the troop. The first males to notice are displaced by more powerful ones until the only one left is the most dominant individual who does not happen to be occupied with another female at that particular moment. He remains close to the female (mate guarding, see Chapter 5) copulating frequently with the result that he fathers her offspring in a high proportion of cases. DNA samples were taken from 213 babies born during the study period and from most of the males and females in the troop, in order to test this direct effect of the hierarchical rank on paternity. Molecular analysis, which is highly reliable, established who was the father of each baby baboon. The results were very clear (Alberts et al. 2006): topranking dominant males had 60% more offspring than the second ranked male, and three times more than the third ranked individual (thirteen levels could be distinguished in the hierarchy, without including the juveniles). Males of the sixth rank or lower produced practically no offspring at all. 4.6.1.1. Competition between human males Our own species also provides examples of all manner of male-male competitions. Thus, direct competition involving violent conflict, which may even end in the death of one of the rivals, has been very frequent throughout human history. At other times competition among men is indirect. History books are full of cases where the powerful disposed of their rivals in order to usurp their women. Surely the most notorious case is that of King David who, the Bible tells us, was captivated by the beauty of Bathsheba, wife of the soldier Uriah, whom he sent to the most dangerous part of the battlefield. Uriah died and thus the king succeeded in acquiring Bathsheba. Such violent mating competition among men remains common today in hunter-gather communities as well as in modern societies. For example, some 40% of Yanomami males have participated in at least one murder and these have twice as many wives and three times as many children as those men who have never killed (Chagnon 1988). Our Western society is no exception here, it is well known that a high proportion of murders are inspired by sexual jealousy. Competition to acquire resources or to acquire a high position in the social hierarchy is also important in our own species. Strong competition exists among men ­ more so than among women ­ for resources and for social status. A positive relationship has been demonstrated between wealth, or social status, and the number of children produced, both in traditional huntergatherer societies and in pre-industrial ones. Nevertheless, some studies have found that this latter relationship does not apply in various modern societies. However, methodological problems inherent in such studies have been identified recently and firm results have been obtained in favour of a positive link between wealth and number of offspring (see Nettle & Pollet 2008 and Chapter 2 for a detailed account). A study that has yielded particularly clear and convincing results was conducted by Daniel Nettle and Thomas Pollet of Newcastle University, UK. They analysed a sample of almost 20,000 people born in England during the week of 3­9 March 1958. They examined educational attainment, salary and number of children at age 46. They found that men with higher salaries had more children that those with lower salaries, and a higher percentage of the latter had no children at all. Also, as in other recent studies (see Chapter 2), they found opposite results for women: those with higher salaries had fewer children than the lower-earners. They also carried out a comparative study in which they calculated an index termed the `standardised linear selection gradient, which allowed the intensity of natural selection on a character to be estimated for the English population and seven other human societies. They found that the selection gradient for wealth in men was lower in modern industrialised societies and higher in subsistence societies (hunter-gatherers, farmers, herders and fishermen), especially in those where a man could marry with several women. Nevertheless, they emphasise that even the lowest selection gradients obtained for this character were similar to those obtained in field studies of other animal species (Nettle & Pollet 2008). That is to say, natural selection has always acted, and will continue to act, penalising those men who are ineffective accumulators of resources or wealth. With respect to competition, the strategy of alliance formation is frequent among male primates (see Chapter 7). In these cases, several males cooperate to overcome another male and acquire his resources or females. Without doubt, such alliances are most frequent and large-scale in the human species. Throughout human history, wars between settlements, tribes or nations have been provoked, more or less deliberately, to deprive neighbours of their resources. The anthropologist Marvin Harris provides much relevant information in his recent book (Harris 2006). Such conflict not only was, and remains, the norm: whole societies specialising in this system of pillage have existed as demonstrated by the Vikings and the Iroquois. In many cases too, another important motivation for conflict has been to steal the adversaries young women, still habitual among the Yanomami today. 35 4.6.2 Male selection by females The female of most species invests much more in her offspring than the male does, as we have indicated. Because the female is going to devote much time and many resources to caring for her offspring, we can expect that she should choose her mate with care. Making the right choice will determine her reproductive success to a large extent. For this reason, females often spend much time in finding a suitable male, irrespective of the energy cost and the risk incurred in moving around to visit several males. Evidence of such active mate-seeking by females occurs in groups as diverse as insects, fish, amphibians, birds and mammals. A study by Patricia Backwell and Neville Passmore, respectively of Natal and Witwatersrand Universities, South Africa, provides a good example. They studied the mate-seeking behaviour of females of the fiddler crab (Uca annulipes). The males live in burrows and the investigators found that females visit several males before making their choice. On average each female visited 7.5 males, although one visited 24 different males (Backwell &Passmore 1996). But on what do females base their choice of mates? We shall deal with this question in the next section. However, it must be stated that although females often do the choosing, it is not always the case. There are instances where males also are selective about their mates and even examples in which the males choose and the females compete for them. When might such a situation arise? Following on from the earlier argument, it is to be expected that the male will be choosy when he too invests in his offspring and that in those species where males care for their young (there are some, though not many) the females will compete for males and the latter will choose their mates (see section 4.6.2.3). 4.6.2.1 What is it about males that females select? Blackwell & Passmore (1996) found that, in the case of females of Uca annulipes that we have just described, mate choice has two stages. Females first decide which male to approach according to his size (they prefer the larger ones). They then decide whether or not to stay according to the quality of the males burrow. This example demonstrates the two types of features that females tend to consider when choosing males (see Box 4.5): resources (the burrow in this case) and good genes (male size here). Therefore, we can answer our previous question in few words. Females base their choice on the benefits that they may obtain (which does not imply a conscious decision; see Chapter 2) and these benefits may be direct (material) or indirect (genetic). 4.6.2.1.1 Direct benefits: resources Females looking for a mate could benefit from acquiring any of the direct benefits specified in Box 4.5, since all of them may increase the number of descendants that they contribute to the next generation. A territory that is food-rich and that offers abundant hiding places and suitable breeding sites will be a good choice. For a female bird, such as the pied flycatcher, evaluating territory quality can be quickly achieved, but obviously this will not always be the case. There are many species whose capacity for movement is limited and these will have to rely on less direct and more subtle pointers when assessing territory quality. A very interesting example is provided in a study by Susan Walls and her collaborators of the University of Southwest Louisiana, USA, of the red-backed salamander (Plethodon cinereus). Walls and her team showed by experiment that females of this species are capable of determining the quality of a males territory by inspecting his excrement. If the remains of poor quality prey, such as ants (which have too much exoskeleton and produce formic acid), abound in these deposits the females will move on. However, if they find a males excrement with remains of more appetising prey, offering more nutrients and fewer toxins, they remain and look for the territory owner (Walls et al. 1989). Direct benefits: Those that bring immediate advantage to the female, such as obtaining resources that she may use to improve her physical condition or her own survival chances or those of her offspring. - A good territory offering abundant resources. - A secure breeding site. - Nuptial gifts. - Parental care by the male. - Fertile sperm. Indirect benefits: Those obtained on a genetic level when the genes of the chosen male are passed to the females offspring which benefit from their fathers `good genes. Known as good gene selection. - An attractive father who will be chosen by a female and who will pass his attractive qualities on to his offspring. - A father of quality, who will be good at competing, avoiding predators and obtaining food, who will pass these qualities to his offspring. - A disease-resistant father, who will pass such resistance to his offspring. - A male whose genes complement those of the female, which will increase the viability of the offspring. Box 4.5. Females choose males according to the benefits that they may obtain from them (which does not imply a conscious decision) and these benefits may be direct (resources needed to raise the young) or indirect (good genes). If females choose males according to the resources that they value, it follows that males will compete among themselves to secure those resources, since these are what will allow them to obtain mates and leave descendants. The females of Lamprologus ocellatus, a small cichlid fish that inhabits Lake Tanganyika, breeds by laying her eggs inside snail shells on the lake bed. Such shells are the most important resource for females whereas the food they eat consists of current-borne particles that are equally abundant everywhere. Thus males strive to obtain shells. Bernhard Walter and Fritz Trillmich, of the University of Bielefeld, Germany, found that each male defends a small territory of about a square metre. He chooses shells and buries them partially in the sand with the openings pointing upwards. Each male endeavours to acquire more shells to bury in his territory. When an egg-laden female arrives, looking for a shell to move into and a male to fertilise the eggs when she lays them, the male unearths one of his shells and invites the female to stay. If she accepts, she moves into the shell and lays her eggs several days later and these are fertilised by the male. A male that owns several shells can continue courting more females. Hence, a fortunate male who owns several shells may fertilize the eggs of several females (Walter & Trillmich 1994). Another type of direct benefit arises when males offer food or another type of nutritive resource to females during pairing (Box 4.5). Bengt Karlsson, of Stockholm University, Sweden, studied copulation in the 36 green-veined white butterfly (Pieris napi) and discovered that a virgin male of this species can deliver a highly protein-rich ejaculate to a female, which is energetically equivalent to the seventy or so eggs that she lays. He was also able to show that the nutrients delivered by the male were used by the female to produce a larger number of eggs (Karlsson 1998). Such nutrient delivery, a kind of `nuptial gift, is common in many insect species. Because the nutrients delivered to a female in the ejaculate tend to be used by her to produce additional eggs, the male investment not only benefits the female but also to the generous donor. He gets to fertilise more eggs than he would if he did not make his nutrient donation. Nuptial gifts may sometimes be more substantial than nutrients transferred during or just before copulation. For example, in some spiders and scorpionflies, courting males present themselves to females bearing the largest and most appetising prey possible. After capturing a good prey item, males of the black-tipped hanging-fly (Bittacus apicalis), a scorpionfly, hang from a twig by their first pair of legs, holding the prey in their third pair. They emit a pheromone, a chemical signal, to communicate their readiness to mate to nearby females that approach and inspect the prey. As shown by Randy Thornhill, of the University of New Mexico, USA, a male may copulate for as long as a female keeps eating, which depends on the size and quality of the prey item. The more prolonged the copulation, the larger the quantity of sperm transmitted ­and therefore the greater the number of eggs fertilized. However, when the prey is large enough, once the mating has lasted for the optimum period to fertilise the eggs, the male tries to make off with what remains of the prey. The female does not cooperate and tries to keep it, leading to a struggle (Thornhill 1976). In some vertebrate species, especially birds, males share in caring for newly-born young (see Chapter 6). In such cases it is clear that it will benefit a female to choose a male who is disposed to invest much time and effort in caring for their offspring. That is to say, selection involves choosing a good father and therein lies the problem: how can a female know whether or not a male will be a good father? This is very difficult to evaluate, but females have shown themselves capable of doing so on many occasions. The selective pressure here is very strong since females who are capable of picking out and pairing with a good father will leave more descendants than those who choose a father who subsequently contributes little to caring for the young. Thus, in monogamous species in which both parents invest in feeding and caring for the young, behavioural norms have developed which inform the female during courtship of the predisposition of a male to be paternal. The nuptial gifts that we have mentioned above are an example. In birds the male frequently brings food to the female during courtship and it has been shown that this does not solely benefit her nutritionally but also allows her to evaluate the males disposition to feed to the chicks afterwards. For example, David Green and Elizabeth Krebs, of Simon Fraser University, Canada, showed that the frequency with which fishes are brought by male ospreys (Pandion haliaetus) to females when courting correlate with their qualities as fathers. The greater the rate of prey delivery to the females, the greater the subsequent delivery rate to the chicks and the faster the nestlings grow before fledging (Green & Krebs 1995). Courtship feeding does not occur in all bird species but recently another way in which a female may evaluate a males paternal qualities has been identified, namely the nest-building behaviour of the male. A high level of involvement in nest building by a male is a good indicator to the female of his predisposition to invest in caring for the chicks (Soler et al. 1998). A bulkier nest will result if the male works a great deal at nest construction, and its size may act as a signal that allows the female to adjust her investment in reproduction. Our research group showed in an experimental study that after manipulating the size of the nests of magpies (Pica pica), the females laid fewer eggs in nests which we had reduced in size and more eggs in those which we had enlarged or in the control (unmodified) nests. Studies such as this show that females judge the males disposition to work at caring for the young, and they lay more or fewer eggs according to this evaluation. 4.6.2.1.2 Indirect benefits: good genes Conceptually the differences between both direct and indirect benefits are clear but it is worth noting that, when it comes to selecting a mate, a female will nearly always base her choice on a mixture of the two types. For example, given that males compete among themselves for territories and, in general, for the resources needed by the females, high quality males genetically speaking, may be expected to acquire the best territories and the best resources. It is therefore very difficult to conclude that a female has based her choice only on direct benefits. The salamander Plethodon cinereus offers a good example. We have used it as a case of how females obtain direct benefits, which it certainly is, but it was no simple matter to demonstrate this. The straightforward observation of males being chosen through their excrement was not convincing proof since these waste material also contain hormones that could serve as indicators of male quality and the female could in fact have been choosing a male for his good genes. The investigators carried out an ingenious experiment on captive salamanders that allowed them to conclude that mate choice was based on direct benefits. The same males were offered ants for a while and later termites over another period. The resulting faeces were collected and presented to females in pairs: one with ant remains and one with termite remains, both from the same male. In this way male quality assessment from the faeces was controlled. The females still preferred excrement with termites, showing that their choice was based on direct benefits (Walls et al. 1989). As defined in Box 4.5, indirect benefits are those that females obtain through mating with their chosen males, whose genes are passed on to the females descendants. Such indirect benefits are less apparent than direct ones. Can a female really derive genetic benefits depending on which male she chooses? The fundamentals of genetics tell us that the offspring of sexually reproducing species receive on average 50% of their genes from their father and 50% from their mother. Hence, if the female succeeds in being fertilised by a strong, fast, agile male who is a strong competitor, a successful forager and good at evading predators, as well as being attractive, then such characteristics may be passed on to the females offspring, which in turn will 37 have increased chances of survival and reproduction, thus resulting in numerous grandchildren for the female. In contrast, were she to be fertilised by a dud male, the chances of her offspring surviving and reproducing successfully would be much reduced and she quite probably would have no grandchildren. In many species the males supply no direct benefits to a female or her offspring but, nevertheless, it is well known that the females do not pair with the first male they meet but rather that they devote time and effort visiting several various males, in order to choose the best one. Since such males only donate sperm to fertilise the female, her choice must be based on what the males genes may contribute to supporting her descendants. But do females really choose males whose genes result in higher-quality offspring? The peacock (Pavo cristatus) has a starring role in debates about sexual selection. Peacock males provide nothing that might appear to benefit a female: they only donate their sperm. Their sole preoccupation is showing off by spreading their spectacular trains when courting females and then to fertilize as many as possible. In the early 1990s Marion Petrie of Oxford University, UK, carried out various studies of sexual selection in peafowl that were living under semi-natural conditions in a park. Her studies revealed that the males with the most impressive trains mated with a greater number of females. In a follow-up study, she showed that males whose fathers had the most striking trains ­ with a greater number of eye-spots ­ grew and survived better than the sons of males with less showy trains. She reached this conclusion by isolating single males and females together at random, thus compelling some females to pair with showy males and others to do so with less attractive ones. To ensure that female quality during brooding had no effect, the eggs were placed in an incubator and once they had hatched all the chicks were raised in captivity under the same conditions. The first interesting result was that the sons of males with most elaborate trains grew more rapidly than those of males with less spectacular trains. Once the chicks had grown she released some of them into the free-living population in the park. She monitored each of them and found that the sons of the showy males survived better than those of the less attractive ones (Petrie 1994). This study thus demonstrated female mate choice for good genes. 4.6.2.2. How do females choose good genes? The peacock example that we have studied in detail is only one of many recent studies which have shown that females choose males on the basis of their genes. Nevertheless, although the idea of obtaining genetic benefits seems quite reasonable, clearly females cannot inspect the males genome directly in order to base their decision on actual genetic information. We can therefore ask two questions: `what do females go on when selecting good genes? and `what mechanisms direct such choices? The answer to the first question is that females base their choice on adornments, the often striking and extravagant structures displayed by males of many species ­ which go under the name of secondary sexual characteristics (see below). The second question is very difficult to answer given that it deals with a highly complex and controversial topic. A long list of mechanisms has been suggested and the results of numerous studies, both observational and experimental, have been published supporting one or other of the various proposals. Still, none is generally applicable, it is difficult to distinguish between them and the mechanisms are not incompatible i.e. several could be acting at the same time in a given species. The following two sections are devoted to these two problems. We shall first consider the secondary sexual characteristics themselves and then the mechanisms proposed to explain the selection of good genes and hence the evolution of those secondary sexual characteristics. 4.6.2.2.1 Secondary sexual characteristics For many species it is easy to tell males from females since they do not look alike. These differences may be the outcome of natural selection, sexual selection or both. Few distinguishing features are solely due to natural selection. An example might be the brood patch, the bare belly region that female birds develop (in species in which incubation is done solely by females) when incubating to allow their eggs to be in direct contact with their skin. Differences due to both types of selection acting together are more numerous. For example, the body size difference between sexes that exists in many species, symmetry and motor coordination are as much due to natural selection as to sexual selection. Undoubtedly, however, most differences and especially the obvious ones are due almost exclusively to sexual selection. These are the typical secondary sexual characteristics which include weaponry (horns, enlarged mandibles, tusks etc.) developed by males in many species for inter-male contests; structural ornaments (tail ornaments in birds, fin ornaments in fish, crests in amphibians) and striking coloration that may or may not accompany these structural features. Secondary sexual characteristics based on auditory and olfactory signals have developed in numerous animal groups. Auditory signals are especially developed in insects, birds, some fish and many amphibians and mammals, whereas olfactory signals are more often exhibited by male reptiles and mammals (see Chapter 11). A final group of secondary sexual characteristics, those based on behavioural displays, is also worth highlighting. These often accompany structural ornamentation and striking coloration since males often perform dances, leaps and other movements, which serve to display their adornments in all their splendour. Sometimes, however, such secondary sexual characteristics may solely comprise an exaggerated and extravagant behaviour without accompanying structures. A good example is provided by the black wheatear (Oenanthe leucura), a bird species in which females base their investment in reproduction on the quantity of pebbles that males are capable of transporting in their presence (see Chapter 2). The most exaggerated and extravagant secondary sexual characteristics occur in species in which the males invest nothing in parental duties whereas in monogamous species, where males collaborate in feeding and caring for the young, secondary sexual characteristics are much more discreet. Furthermore, in those species where the males invest in parental care and are themselves selective in mate choice, the females too may develop more or less exaggerated ornamentation. Why do females select males according to the latters secondary sexual characteristics? In the case of the black 38 wheatear above, it is evident that the male demonstrates his physical fitness and disposition to work through his pebble-carrying display. More generally, secondary sexual characteristics are indicators of fitness or quality. Most studies show that females choose them because they are honest indicators, which implies that they must be costly to produce and maintain. Clearly pebblecarrying is costly for the male black wheatear since it requires considerable energy consumption. But what about brightly coloured and extravagant ornaments? They too are costly and in more ways than one. First, they may make an individual more conspicuous to predators. Also, developing such adornments may consume essential nutrients that have other specific functions, for example in defence against disease and parasites (see `the immunocompetence handicap hypothesis in Box 4.6). A relationship between exaggerated ornamentation and reduced survival chances is to be expected since the former poses problems of camouflage and escape from predators. Nevertheless, where this has been studied it has been found that within a given species those males with the most highly developed ornaments are those which survive best (Jennions et al. 2001). This is because secondary sexual characteristics are honest indicators of quality and hence individuals with the most extreme ornaments are also the best survivors despite producing a trait that is costly to make and maintain. Thus, the only way to demonstrate that ornaments are indeed costly and have a negative effect on viability is by an experiment in which individual quality can be controlled. Anders Møller of Pierre et Marie Curie University of Paris, France, and Florentino de Lope of the University of Extremadura, Spain, carried out an ingenious experimental study on the barn swallow (Hirundo rustica), in which they demonstrated the costs associated with the exaggerated tail shown by males of this species whose tail is some 20% longer than in females. Earlier studies by Anders Møller and his coworkers had already shown the importance of the tail in the context of sexual selection. Thus, for example, longer-tailed males succeeding in pairing earlier and with higher quality females and, in addition, they were the ones who most often indulged in extra-pair copulations (i.e. mating with females other than their mates. See Chapter 5). To determine whether the long tail incurred a significant cost independently of male quality, they manipulated tail length. Males were divided into three groups: the tails of one group were shortened, those of another group were lengthened and those of the third group were untouched. Thus males had tail lengths that were unrelated to their own quality, since the type of treatment received by each individual was decided at random. Once the experiment had run its course they found that males with lengthened tails had less chance of being alive the following year than those whose tail had been shortened. They concluded that a longer tail is costly for male swallows (Møller & de Lope 1994). 4.6.2.2.2 Why have multiple adornments? Males of different species very frequently exhibit more than one type of ornament. An exaggerated structure is usually accompanied by striking colours and some kind of acoustic signal. One of the ornaments normally Since we began considering sexual selection we have been applying the general arguments that are the basis of the theory. For example, females invest more than males in reproduction and males may increase the numbers of their descendants by mating with more females, whereas overshadows the rest but sometimes there may be several highly developed types. The most extreme example is surely the lyrebird (Menura novaehollandiae), a large Australian passerine bird. The male has a majestic lyre-shaped tail formed by the two external tail feathers and twelve central ones comprising a fine tracery. He also has a very showy appearance with grey, brown and white markings. Male lyrebirds do not contribute at all to caring for the young and instead dedicate all their efforts to attracting and pairing with as many females as possible. They establish a small area on the forest floor which they keep clear of leaves and twigs and where they perform their displays. When a female appears they raise their tails so that the feathers form a lacy veil over their heads. They then begin to perform an elegant dance, all the while emitting the most varied vocal repertoire, which includes imitations of many of the sounds of the forest, from the song of other species to the sound of a chainsaw. Since an ornament may be an honest indicator of male quality, why have multiple ornaments? We are still far from answering that question but three possibilities have been proposed to date. Firstly, perhaps each type of ornament provides information on a different attribute of the male. Secondly, different secondary sexual characteristics may provide redundant information but may enable the honest signal to be evaluated more easily by the female. Finally, some of the characteristics may provide no relevant information at all about the male and instead may be evolutionary relicts of ornaments that were functional in the past. 4.6.2.2.3 Mechanisms proposed to explain mate choice for good genes The topic of mate choice for good genes has attracted much investigation and various alternative hypotheses. Nevertheless, although all these explanations have attracted some support, none so far has been so broadly applicable as to be regarded as definitive. Attempting to analyse the various ideas by commenting on examples of the experimental studies supporting each of the hypotheses would lengthen this chapter excessively. Thus I have opted for Box 4.6, where the theoretical background is treated in more detail than usual, and less attention is given to the topic in the text. Fishers runaway selection model suggests that a female will select a very attractive male simply because her offspring will then also be attractive and will be selected by many females and leave her many grandchildren. The alluring character need not be an indicator of anything, it need only be attractive to females. In contrast, models based on mechanisms indicating good genes assume that the offspring of a female who has been fertilised by an attractive male will not only be themselves more attractive but they will also have inherited other advantageous characteristics that will allow them to enjoy greater chances of survival. 4.6.2.3. It is not always the males who compete and the females who choose 39 females can only increase their reproductive success by choosing higher quality males and securing the best resources. The runaway selection model: This model, proposed long ago by Ronald Fisher, suggests that females select attractive males, that is those with highly developed secondary sexual characteristics, not because these are indicators of good genes but simply because they are attractive. He proposed the existence of a genetic relationship between the genes that determine the preference of a character by females and those genes that determine the development of that character by males. This genetic relationship would be mutually self-reinforcing, favouring very rapid evolution (which is why it is described as `runaway). Mechanisms indicating good genes: This group includes various models whose starting point is that features which make males attractive are indicators of genetic quality (see the peacocks train example in section 4.6.2.1.2). In order to be honest indicators such features must be costly to develop and/or maintain. An important theoretical problem here is that such mechanisms imply very strong directional selection, which is to say, if males with the most exaggerated characters are always selected, genetic variability will soon disappear, which would mean that females gain nothing by being choosey. This has been termed the `lek paradox since it is especially striking in species that pair at leks (see Chapter 6). - The handicap principle: Amoth Zahavi proposed that the most exaggerated ornaments are burdens that reduce the survival of the males which bear them. Hence, a male whose ornamentation is more exaggerated than that of other males is indicating that he is very fit since he is capable of surviving despite the handicap of his ornaments. - The parasite-resistance model: William Hamilton and Marlene Zuk suggested that attractive adornments and showy colours indicate the absence of parasites to the female and hence that the male has parasite resistance that he may transmit to his descendants. This model offers a possible solution to the lek paradox given that parasites differ each year and in each area and so resistance to them would not be uniform. - The immunocompetence handicap hypothesis: This proposes that since the development of ornamentation is under the influence of the endocrine system, investing heavily in such adornments may prejudice the immune system. There are two important versions of this hypothesis. One is related specifically to testosterone, a hormone that has the effect of exaggerating sexual display behaviour while also having a negative influence on the immune system. The other is related to carotenes, the pigments responsible for structures coloured yellow or red. Carotenes are not manufactured in the body but have to be ingested in the diet, thus an important trade-off exists between dedicating these chemicals to sexual signals or to their important role as antioxidants. - The fluctuating asymmetry model: Many studies, both descriptive and experimental, have shown that in a great diversity of organisms (insects, fish, birds and mammals) the females select symmetrical males (those with a low level of variable asymmetry) and hence the greater the symmetry of a male, the greater his attractiveness, and consequently the higher his reproductive success. The biological justification for the preference for symmetry is that, in theory, an individual who has grown up in perfect conditions should be entirely symmetrical. Hence any deviation from perfect symmetry would be the outcome of problems encountered during development and indicate that a potential partner could be defective in some way. Genetic compatibility mechanisms: It has been demonstrated in diverse organisms, humans included, that females may select males on the basis of their genetic complementarity (the match between the male and female genomes) because this brings advantages in the form of greater fertility and increased viability of progeny. The clearest results have been obtained in studies of the Major Histocompatibility Complex (MHC), a group of linked genes strongly associated with the immune system and resistance against disease. ORIGIN Direct phenotypic effects: As Fisher suggested, females may begin choosing a male adornment because, at first, this structure could offer a direct benefit. For example, in a bird a slightly longer tail might experience some advantage in flight. Also an ornament could indicate certain abilities of a male when the time came for it to carry some material benefit. Exploitation of female sensory biases: A male ornament may confer an advantage simply because it offers something that females already tended to seek. That is to say, if for whatever reason females prefer some existing characteristic, be it for its form or colour or whatever, that males with that character will be preferred as soon as they happen to acquire it. Box 4.6. Some of the most important mechanisms proposed to explain the selection of males by females based on genetic benefits. Two hypotheses that may explain the origin of secondary sexual characters are also included. These are general rules but it is important to emphasise that they do not always apply, for two reasons. Firstly, there are exceptions that do not contradict sexual selection theory but instead support it, since they fulfil predictions derived from it. Secondly, because recently published studies have shown that, contrary to the standard view, both competition between females for access to males and mate-selection on the part of males are more frequent than was supposed (Clutton-Brock 2007). An impressive study relating to the second point is the work by Leah Domb and Mark Pagel, of Harvard University, USA, and Reading University, UK, respectively, on sexual selection in the yellow baboon. In this species, as noted earlier in this chapter, females in heat develop a striking pink genital swelling. The authors thought that this could comprise an ornament indicating female quality, similar to the very different ornaments exhibited by males. They found that the females with the largest swellings began breeding earlier and their offspring had better survival prospects than those of females with less developed swellings. They therefore concluded that the swelling is a sexual ornament that indicates a females reproductive potential. Accordingly they also found that males fought longer over the females with the most prominent swellings. An important question is `why do females develop a costly ornament ­ it may amount to 14% of their body mass ­ that indicates their quality honestly, as do those of males, if it is the females who do the selecting? The answer suggested by the authors is that given that contests between males are costly, such a signal serves to motivate a dominant male who may already be with a female in heat. A female who displays her greater reproductive value may ensure that the best males compete for her and that her offsprings parent will be the fittest male of all (Domb & Pagel 2001). In accordance with the first reason given above, there are important exceptions to the general rule that males compete and females select, which nevertheless do not contradict sexual selection theory. It is certainly the case that when males make a significant parental investment, it may be predicted that such males will not accept just any female. We can also predict that in such circumstances it will be the females who will fight among themselves to acquire a preferred partner. This most extreme case of this sort is known as `sex-role reversal. A particularly striking example is provided by the jacanas, members of the bird family Jacanidae. Sexrole reversal has been documented in seven of the eight jacana species. In these the males perform all parental care, including incubation and care of the chicks. The females, who are substantially larger than the males, fight among themselves and defend large, food-rich territories. Within a females territory, the males defend their own territories against other males. If a females territory is sufficiently large and rich in resources it may include up to four male territories, that is to say the female possesses a `harem of four males. She will copulate with one of them and lay a clutch for him to care for. She will then lay another clutch into the care of another male, and so on successively (an instance of polyandry; see Chapter 6). The above examples allow us to draw a very important general conclusion: although normally males compete and females select this is not always so but rather depends on the parental investment of either sex. If males invest more than females, it is the males who will be selective and if it is the males alone who care for the young, they will be as selective as the females of those species where care for the offspring is a female 40 responsibility. In such cases it will be the males who are selective and the females who compete for mates, the opposite of the more general situation. Nevertheless, where both males and females invest in parental care, both sexes may evolve mate choice behaviour and both may evolve appropriate secondary sexual characteristics. 4.6.3 Mate selection in humans This topic is highly controversial. The approach presented here may even damage romantic sensitivities. Therefore I want to begin by clarifying two points. First, mate-seeking in our own species, both in the short and long terms, is not wholly a conscious decision. Secondly nobody should take what we conclude in this section personally; although we make generalisations here, remember that they are always from the point of view of statistical tendencies and there may be many exceptions to the general rule. The first point, that not all human decisions need be conscious ones, needs to be clearly understood and is worth dwelling on briefly. To make this point, we shall examine a now famous study that was carried out by Claus Wedekind and his co-workers at the University of Berne, Switzerland, who examined the influence of the Major Histocompatibility Complex (MHC; see Box 4.6) on pair formation in humans. Couples with varied MHC genes are capable of producing children who have a greater diversity of defences against parasites than do those whose genes are more similar. Hence, if a female were able to choose a male with an MHC distinct from her own, she would tend to have children who were more resistant to diseases and parasites. This idea had received strong support from a study of mice (Potts et al. 1991), and Wedekind and his team designed an experiment to see whether there was a similar effect in humans. The study was carried out on students of their own university. Males were given a T-shirt which they were asked to wear for two consecutive nights and during this period they were not to wear either deodorant or perfume nor were they allowed to drink alcohol or smoke, or do anything else that could mask their personal body odour. After this the members of a group of females were each given six of the T-shirts and they were asked to rank them according to how attractive they found their odour. The investigators found that the most attractive T-shirts to those females who were not taking contraceptive pills were those worn by males whose MHCs were most different from their own. Moreover, the odour of males whose MHC was most different resembled that of the females current partner more closely than that of males whose MHC was more similar. This finding provides quite strong support of the fact that the MHC can also influence unconscious mate choice by women today. What I wish to emphasise after describing this example is that the women who took part in the T-shirtodour study were unaware of both the identity and the appearance of the T-shirt wearers, still less were they able to compare the MHCs of the latter with that of their current partner. This example thus allows us to conclude that even in our own species, which we like to regard as intelligent and conscious of everything we do and decide, in these matters ­as in many others- we very often take decisions that are not entirely based on reasoned evaluations and conscious reflection. Often even the most preconsidered decisions are based, at least partly, on evolved psychological mechanisms that supply adaptive solutions for the problems implicit in reproduction. After all, todays humans are the descendants of ancestors who were successful when it came to producing surviving offspring. Leaving progeny is no easy matter since, among other things, it requires finding a suitable mate, competing with same-sex rivals and ensuring that conditions are right for raising offspring successfully. Therefore, the selective pressures that have acted over the long period of human evolution should have given rise to numerous psychological and behavioural adaptations that shape how we behave when pairing off and reproducing. In order to understand human pair-selection strategies we need to bear in mind the theoretical considerations emphasized throughout this chapter since these explain a large part of the strategic differences between men and women. For example, in accordance with the general rule, since human males, along with those of most other species, produce large amounts of sperm, they could increase the number of their descendants by impregnating more women. In contrast, women produce a limited number of ova and cannot increase the numbers of their offspring by increasing the number of men with whom they have sexual relations. Instead, ours is a species in which the females, in accordance with the general rule, invest considerably more than the males in producing descendants, although human males, unlike those of most other mammals do participate in parental care. The theoretical considerations highlighted above indicate that although natural selection will favour those men and women who leave most descendants, the two sexes should have different strategies for achieving this since they are subject to different selective pressures. Women may attain this outcome if they choose men who make an effective contribution to parental care or whose genetic contribution is of high quality. Men, on the other hand, will maximise their reproductive success by impregnating as many fertile women as possible. Applying this evolutionary theoretical framework has reshaped the intellectual and scientific environment of the academic discipline of psychology. It has resulted in hundreds of hypotheses and predictions that have been translated into thousands of papers in specialised scientific journals, which are making a major contribution to helping us to know ourselves much better. This new approach has given rise to the discipline known as `evolutionary psychology. Before studying human pair selection, the most interesting aspect of sexual selection, we shall examine one of the most general predictions that arise from the theory we have studied. It may be predicted that, as with most males of other species, men will have a greater predisposition to have sexual relations with many women, whereas this promiscuous tendency will be much less marked in women. Is this prediction fulfilled? The answer is a resounding yes and many studies support it. One of the most conclusive was an experimental study published by Russell Clark of Florida State University, USA, and Elaine Hatfield of Hawaii University, USA. They enlisted a group of attractive youths of both sexes to act as lures. Each of these young people, very smartly dressed, would approach another youngster of the opposite sex who happened to be alone. 41 After an opening line of `Hello, Ive been seeing you around the campus and I find you very attractive, they would ask one of the following three questions: (1) `Would you like to go out with me?, (2) `Would you like to come to my apartment?, or (3) `Would you like to have sex with me?. There were no differences between boys and girls in the replies to the first question (50% said yes in both cases). However, the responses to the other two questions were very different, in accordance with our initial prediction. Only 6% of the young women answered yes to the invitation to the apartment and none at all (0%) accepted the direct offer of sex. In contrast, 69% of boys accepted the offer of accompanying the girl to her apartment and 75% agreed, probably enthusiastically, to have sex with her (Clark & Hatfield 1989). These results clearly support the prediction that men are always more inclined than women to have sexual relations. 4.6.3.1 What do women and men choose when looking for a permanent partner? Mate-seeking strategies are complex in human beings but in general both men and women exhibit two distinct types, those culminating in long-term relationships and those leading to brief sexual encounters. We shall deal with the former in this section, those strategies that give rise to more lasting relationships within which normally children are born and raised. Such lasting relationships may begin as a result of what we call `falling in love, a favourite theme that has inspired poets and artists and one long regarded as among the most sublime sentiments of the human soul. We may, however, need to lower the concept of love to a less sublime and more earthly level. First of all, what does falling in love entail? No doubt most of you have been in love and you will have your own particular answers to this question ­ all of which will be correct. For two people to fall in love means: attaining the seventh heaven, living in a permanent state of euphoria, unleashing a tempest that disrupts and upturns their lives, a rebirth of youth (in more mature couples), an avalanche of joy and enthusiasm, and so on. Still, let us examine it coolly from a more distant viewpoint, that is to say, without reference to ourselves but rather as we see others who are in love. We tend to say that they seem crazy and that they neither know nor care what they do, although we also tend to add that they seem very happy. How would an impartial observer describe love? Imagine an extraterrestrial scientist who sets out to observe human couples in love. After studying a sufficient number of cases over a long-enough period he would no doubt describe their state as a transitory deviation from the norm characterised by a very high frequency of copulation, a certain generalised hyperactivity and a reduced need for sleeping and eating, all worthy of psychiatric investigation. With that I think we have lowered love from its romantic pedestal but we can lower it still further if we ask ourselves what are the physiological causes of this state of mind. Neuroendocrinology has made enormous advances in this field and without going into the details, we can say that falling in love is chiefly directed by neural pathways whose principal chemical neurotransmitter is dopamine. This is to say that the pathways involved are those of the brains gratification systems (Tobeña 2006). Hence the adaptive mechanisms of the brain are responsible for lovers feeling happy and besotted with one another. What makes one fall in love? I doubt that anyone believes in Cupids arrow, but when you ask people why they have fallen in love with their chosen partner they are uncertain and find it very hard to reply. If furthermore they are asked why they fell in love with this particular person and not with one of the many others whom they knew at the time when they will be unable to answer ­ each of you can try this exercise with respect to your partner. True love, in which one person rather than another bowls us over at a particular moment, is chiefly an instinctive response to a complex series of stimuli provided by the beloved. We can nonetheless study pair-seeking strategies in both sexes. These are highly diverse and they vary not only between men and women but also according to whether a companion is being sought for a long-term relationship or for a casual sexual encounter. In addition, various factors influence the selective behaviour of both sexes: nationality or culture, the sex ratio (the number of women divided by the number of men who are seeking mates), the richness in resources of the area and the risk of contracting infectious diseases. None of this means however that it is impossible to generalise since many clear strategies are detectable in all human populations, independently of geography, culture and other factors. A great deal of information exists on mate-choice in humans. The abundant published studies generally involve either circulating questionnaires with a series of questions comprising the object of study or analyses of mate-wanted advertisements in newspapers or on the Internet or statistical studies of some aspects or experimental studies such as the one in the previous section. Box 4.7 sets out ten characteristics that stand out as the most important for mate-selection in both men and women, specifying their relative importance to either sex and the degree of their universality, i.e. whether or not they figure in all cultures. We shall then examine one of the most interesting aspects from this box. CHARACTERISTIC IMPORTANCE TO MEN (0-3) IMPORTANCE TO WOMEN (0-3) IS IT UNIVERSAL? (YES IF FOUND IN MORE THAN 95% OF CULTURES) YES YES YES YES YES YES NO YES YES YES Wealth and resources Possibilities for acquiring resources Ambition and competitiveness Height and strength Beauty and physical attractiveness Youth Virginity or chastity Intelligence Likeability and understanding Being a good person 1 1 0.5 0 2.8 3 1.6 2 2 2.3 2.5 2.5 2.5 2.5 1.5 0 1.3 2 2 2.3 Box 4.7. Characteristics used in mate-selection by women and men. The relative importance of each characteristic when choosing a mate is specified (on a scale of 0­3). The universality of that characteristic, i.e. whether or not it applies generally and arises independently of culture, is also given. Information based on diverse sources but principally on the study of 37 different cultures by Buss et al. (1990). 42 All the characteristics display the trends and relative importance predicted by evolutionary theory, both for males and for females. Before going into details, a general finding is that all those characteristics related to the selection of direct benefits (resource availability, possibility of acquiring resources, the ambition and competitive of a potential partner) are much more highly regarded by women than by men, whereas characteristics related to physical attractiveness are more highly valued by men than by women (Box 4.7). Dozens of published studies support these general trends, which apply to all nations and in those indigenous communities where they have been studied. By way of example we will consider a study by I. A. Greenlees of Stirling University, UK, and William McGrew of Miami University, USA, based on an analysis of the `lonely hearts advertisements of a newspaper. They found that women sought financial security more often than men did (33% of women v. 9% of men) and that in their own advertisements men offered financial security more often than women did (69% v. 43%). Physical attractiveness was sought by 49% of men and 33% of women but was offered by 71% of women and 50% of men (Greenlees & McGrew 1994). This study thus shows that not only are resources more important to women than to men, and physical attractiveness more important to men than to women, but also that each sex offers what the other chooses with greater frequency. The two characteristics in the summary in Box 4.7 which differ most in the preferences of men and women are height and strength, which women clearly select (for a women the ideal mate is a man taller than herself where for a man a shorter woman is preferred), and youth, which only men select preferentially. Height and strength offer both direct and indirect benefits to women. A tall strong man would bring her more effective protection against enemies and predators but, in addition, would bring her genetic benefits since her offspring could inherit these positive attributes. All studies also show clear differences between the two sexes regarding the preferred age of their mates. A woman prefers a man older than herself but a man chooses younger women. Both tendencies are directly predicted by evolutionary theory. Women prefer older men because these already have the experience, status and accumulated wealth that permits them to provide greater resources for their children. Men prefer younger women since these are more fertile and hence of greater reproductive value. Several studies have supported these predictions. A recent work by Samuli Helle of Turku University, Finland, and his collaborators has produced very convincing results. They analysed the registers of weddings, births and deaths in the Lutheran churches of northern Finland, a region inhabited by the Sami, a people that lived from their reindeer herds, hunting and fishing. They were monogamous since they were prohibited by law from remarriage except after a spouse died. The researchers analysed the data for 706 couples who had only married once. Each couple produced 5.6 children on average, with a range from one to fourteen. The most fertile couples were those where the man was about 15 years older than the woman. This is a substantially greater difference than that found in other similar studies, where the range is from two to six years, probably because of the special characteristics of the Sami population. The authors concluded that 15 years was the optimum age difference since it implied that an older man, with accumulated wealth and the experience needed to be a good hunter and fisherman, who married a very young woman was able to enjoy a long reproductive life with his youthful partner (Helle et al. 2008). Another noteworthy feature of the information in Box 4.7 relates to the final three characteristics. Both sexes prefer intelligent, likeable and compassionate people with a well developed moral sense; in other words, good people. These characteristics were not greatly considered by early studies on human mate choice but they have gained importance in more recent work, so that it is now suggested that both intelligence and cognitive capacity (Miller 2000) and moral virtues (Miller 2007) have evolved as a consequence of selective pressures arising from the need to find a mate. There are two particularly enigmatic and controversial aspects of mate selection in humans. One is the fact that men choose beauty and the other that women sometimes accept (and sometimes seek) sexual relationships without a long-term commitment. We shall consider the first of these here and the second in the next chapter. Why do men choose beautiful women? Clearly this preference is more than a whim. If it is the outcome of selective processes it implies that men who succeed in pairing with beautiful women derive reproductive benefits. And what exactly do we mean by a beautiful woman? This is hard to sum up in a few words but the fact is that all men know a beautiful woman when they see one, without any need for instruction. Diverse studies, both geographically and culturally, have shown that men need no more than a brief glance to assess the beauty of a face or a figure and they do so with a high degree of concordance. What is most remarkable is that the evaluations are highly similar irrespective of the race of either the men doing the assessing or of the women being assessed. Hence, contrary to the assertions of some anthropologists, the concept of beauty does not seem to differ significantly between cultures. The principal features highlighted by different studies as the components of the general concept of beauty are fleshy lips, a small chin, soft and unblemished skin, lustrous hair, white teeth, firm breasts, symmetrical features, a feminine aspect and a low waist-hip ratio of about 0.7 (i.e. a narrow waist and wider hips). What do all these features have in common? They are all indicators of good health or youth, and these together imply a high reproductive value. Female beauty is thus not defined by an arbitrary collection of features but instead beautiful women are potentially more fertile and may give a man more children than would less attractive women. These general strategies of mate-choice in humans which, as we have seen are clearly predicted by evolutionary theory, in turn explain many typical phenomena of human societies. For example, as a result of men seeking health and beauty, women spend a great deal of money on anti-wrinkle treatments, collagen injections and cosmetic surgery, among others, all these amounting to an industry worth many millions in hard currency in the industrialised countries. Men in turn have developed an instinctive ambition that drives them to accumulate wealth and resources, since these are what women have looked for in them over thousands of 43 generations. As a general rule, men are much more ambitious and avaricious than women. All these are general rules but it is indeed the case that there has been a recent upsurge in ambitious female executives and in those males known as `metrosexuals, who also spend large sums on cosmetic treatments. It is too soon to analyse these phenomena from the point of view of mate selection but they may be currently adaptive cultural modifications in which economically independent women may be choosing male beauty instead of resources (see Section 4.6.3.4). 4.6.3.2 Casual sexual relationships As we have already emphasised, given that males have much more to gain than females from copulating with many individuals, evolutionary theory predicts that the former should be much more promiscuous than the latter. This is indeed what occurs in the human species. For women, as for females of other animals, increasing the number of mates does not increase the number of offspring, yet casual sexual relationships are relatively frequent in our species (see Chapter 5). Such relationships were obviously advantageous for men during the Stone Age, given that raising a child is very costly (nine months of pregnancy are followed by a minimum of 12­15 years feeding and caring for it). Promiscuous males may avoid this costly investment. However, it is hard to understand why women consent to casual sex with a nonpaternal male. Several hypotheses have been advanced to explain why women have casual sexual relationships, all of which have some substance and explain some cases. There are four principal explanations. The `deception hypothesis suggests that women accept a casual sexual relationship because they are tricked by men with promises of long-term commitment that are never fulfilled. The `additional resources hypothesis suggests that such copulations allow women to obtain additional resources from men, which occurs today in huntergatherer societies, such as the Aché, of Paraguay. The `mate-change hypothesis suggests that such copulations are an attempt by a woman to change her current mate for a better one. Finally, the `good gene search hypothesis maintains that such sporadic sexual relationships, when a women already has a mate, bring her the opportunity to have more diverse offspring of higher genetic quality, which is advantageous as we have seen. Women give more importance to physical attractiveness for casual sexual relationships than they do when they are looking for long-term relationships (in accordance with the final hypothesis above), preferring men with more masculine features such as tall, broadshouldered, narrow-waisted and muscular. This means that such men should be more involved in such casual relationships, something that has been confirmed by other studies. For example, Gillian Rhodes and her team at the University of Western Australia studied a sample of 166 men and 196 women. They found that the more attractive men had more casual sex but not more longterm relationships. For their part, the more attractive women had more long-term relationships but not more casual ones (Rhodes et al. 2005). This shows that the women who permit casual sexual relationships are not the more attractive ones. 4.6.3.3 Human secondary sexual characteristics As we have already mentioned, human males also participate in mate choice since they too contribute to parental care or at least provide some family resources. Secondary sexual characteristics may therefore be predicted to occur in both sexes, although they would not be expected to be as spectacular as those of males of more polygynous species. The differences between males and females are certainly varied and important and some could be considered sexual ornaments. The principal candidates are the penis and the high waist­shoulder ratio in men, and the breasts and low waist­hip ratio in women. The existence of secondary sexual characteristics in humans is not at all clear given that the features that we have studied and which tend to be the basis of mate selection by women, such as greater height and a combination of broad shoulders and narrow waists, are neither ornamental nor still less costly but instead are indicators of strength, which have evolved through natural selection. The human penis may be a secondary sexual characteristic since it is very large relative to that of other primates ­about twice as large as in the chimpanzee and four times larger than in the relatively immense gorilla. The penis might be a costly ornament since the larger the penis, the more blood needed to erect it. However, most authors do not regard the large penis as a secondary sexual characteristic given that its size and other features may be explained by the other benefits that they may bring with respect to fertilisation and sperm competition. Hence we shall defer our study of it to the next chapter where we examine those two topics. There is more evidence for regarding the two female features mentioned as secondary sexual characteristics. The broad hips ­ narrow waist relationship may be considered a sexual ornament since it leads to the curvy figure and distinctly feminine walk which so appeal to men. Wide hips do not indicate easier birthing. Indeed they may be a costly attribute since they make rapid movement more difficult, making it harder to escape certain predators. Female breasts are unanimously regarded as a secondary sexual characteristic. They are very large relative to those of females of other primate species, and they remain much the same size throughout the reproductive cycle whereas in other species they are only prominent during lactation. They do not bring any other type of advantage but rather incur a cost since they make running harder. Thus wide hips ­ narrow waists and prominent breasts may act as secondary sexual characteristics, indicating youth and a high reproductive potential. Is there any scientific support for this last assertion? Several studies do indeed support this hypothesis, especially with regard to breasts. Anders Møller of Pierre et Marie Curie University, Paris, France; Randy Thornhill of New Mexico University, USA, and myself have shown that women with more symmetrical breasts have more offspring and similar results have been obtained from two very different populations, in Granada in southern Spain and in New Mexico in the southern USA (Møller et al. 1998). The relationship between symmetry and fertility indicates that breasts may serve as honest indicators of good genes. These results have been confirmed and extended in a later 44 study by Grazyna Jasieska of the Jagiellonian University, Poland, and her collaborators, who analysed the relationship between the dimensions of various body parts and fertility. The latter was measured from the daily concentration of two hormones in the saliva, whose link to the success of pregnancy had previously been shown. They found that women who had both large breasts and slim waists had a higher concentration of both hormones, 26% and 37% higher respectively, than other women, indicating that the former are more fertile (Jasieska et al. 2004). To end this section on human secondary sexual characteristics I would like to suggest one that may apply to both sexes but that I have never seen mentioned in the literature: the growth of long hair on the head by both men and women and, in addition, beard growth in men. These characters meet all the requirements of sexual ornaments. Long hair is an exaggerated and extravagant adornment that may reveal the quality of its bearer (high quality individuals have more presentable hair since they can spend more time looking after it). Furthermore, as with typical secondary sexual characteristics, it is costly to maintain. Not only does it take longer to look after but it can also amount to a handicap since it may shelter more parasites and may also prove a problem both when trying to escape predators and during fights with rivals of the same sex. 4.6.3.4 Sexual selection in modern industrialised societies As we have already emphasised in this book, human behavioural evolution took place during the tens of thousands of years that comprised the Stone Age, during which time our ancestors lived as hunter-gatherers. The society currently typical of industrialised countries is very recent indeed in evolutionary terms and perhaps there has not been enough time for adaptations to our present living conditions to emerge. Thus the adaptive significance of the human sexual behaviour complex must be sought in the ecological environments that our ancestors lived in. One of the adaptations that has frequently been demonstrated is the flexibility of mate-seeking strategies. When seeking a partner, males as much as females, adapt their requirements to the prevailing circumstances. For example, an individuals concept of his or her own worth as a mate has been seen to be very influential. The number of potential mates available has also been shown to be equally important. This adaptive flexibility should allow us to predict that changes ought to be detectable in pair-selection strategies in industrialised societies, which have seen enormous changes in the living conditions of both sexes, particularly with respect to the high percentage of women who are economically independent. Have any such changes been detected? They have indeed. A group of Spanish investigators, Carlos Gil-Burmann and his co-workers at the Universidad Autónoma de Madrid, have come up with some very interesting results through an analysis of `lonely heart advertisements in a range of Spanish periodicals. They have uncovered an age-related difference in the advertisements that are published by women looking for a mate. In keeping with the general rule, 52.3% of women over 40 seek a partner of high socioeconomic status and they attach less importance to physical attractiveness, which is specified by only 40.1%. However, 50.7% of women under 40 seek attractive men and they give less importance to financial status, required by only 46.4%. 4.7 Male-female conflict in mate choice We have already highlighted that males and females do not invest equally in reproduction, it pays males to dedicate their efforts to acquiring as many mates as possible, whereas parental investment is the best strategy for females since they have little to gain from additional sexual partners. This implies that the selective pressures affecting each sex are different and thus that the evolutionary interests of males and females are highly distinct. As a result, it is increasingly evident that intersexual conflict is the norm and not the exception and that such conflict gives rise to `antagonistic coevolution (see Chapter 9) between males and females. This coevolution has led to the emergence in each sex of defensive evolutionary strategies against potentially harmful members of the opposite sex. As a general rule we can say that in most species the males develop strategies to deceive the females and the females develop strategies to prevent themselves being taken-in by deceptive males. Conflicts between males and females are numerous and occur at various levels. The most widespread cause is that when it comes to finding a mate not all individuals will be able to pair with the partner of their choice. Not all males can pair with higher quality females nor can all females pair with the best males and/or those who control more resources. This conflict resolves itself in nature, in species that form lasting pairbonds, through what is termed `assortative mating, that is to say there is a tendency for males and females to pair off with mates of similar quality, and humans are no exception here. One of the extreme consequences that may arise from intersexual conflict is that large males may try to force smaller females to mate with them. Such attempts are quite frequent in the animal kingdom and include such behaviours as bullying, intimidation, kidnapping and forced copulation (rape). Forced copulations are comparatively rare but they occur in diverse species of ducks and geese, and in some insect, fish, amphibians and mammals, including a number of primate species in addition to humans. Undoubtedly the fullest study of rape is that by Randy Thornhill, of the University of New Mexico, USA, on scorpionflies (Panorpa spp.). The males of these predatory insects tend to court females with a nuptial gift, which may be a prey item or a secretion from their salivary glands. Nevertheless, a male will sometimes approach a female without offering a gift. When he is close to her he leaps on her and tries to secure her with his abdominal pincer. Female try to avoid males of this sort by fleeing when a giftless male approaches and, if held fast, they struggle violently to try and escape. If the male succeeds in holding on to his victim he will try to grip his genital pincer against the females genitalia in order to begin copulation, which may last for several hours in some species. Such forced copulations were observed in nearly all of the 18 scorpionfly species that Thornhill studied in the laboratory but it is not solely a phenomenon resulting from the conditions of captivity, since he also observed it in seven species under natural conditions (Thornhill 1980). The strategy of these males is clearly 45 prejudicial to the females but it does benefit the males since their way of finding gift food consists of removing prey from spiders webs, a very risky business since approximately 65% of males get trapped in webs. By not presenting a female with a gift the male lessens the chance of dying in a web. If therefore simply grabbing a female is much less costly to a male, why do the majority court females and only a few carry out forced copulations? Probably because forced are usually ineffective. Because females control fertilisation, they have developed defensive mechanisms to avoid or reduce the chance that a rapists sperm will be the ones that fertilise her eggs (see Chapter 5). That being so, it may be predicted that the rapists are males of low quality, those who are incapable of providing a nuptial gift adequate to attract a female. Rape is widespread in the human species, but more frequent in some societies than in others. For example, rape is very rare in Norway but more frequent in the United States (with 60,000 instances reported). In some ethnic groups, such as the Aché of Paraguay and the Yanomami and the Mehinaku of the Amazon jungle, rape is very common (Buss 2007). Although there are important inter-cultural differences in the frequency of rape, no culture has been found in which rape is absent. Even the Bible is laden with accounts of men raping women. Rape has been studied from many viewpoints (anthropological, psychological, sociological and biological), and various ideas have been advanced to explain why it occurs. Some have argued that rape may simply be a way in which a male obtains sexual gratification. Others claim that sexual violence enables a man to impose his will on a woman. Alternatively to those proximate hypotheses, it may be an adaptive behaviour, an outcome of biological evolution, which may improve the reproductive success of the rapist. Although rape certainly involves the sexual gratification of the rapist, and forced copulation implies considerable violence that, from a psychological viewpoint, may promote feelings of dominance in a man, much data supports the last hypothesis (extracts from Thornhill & Palmer 2000; Buss 2007). Some data indicate that rape is adaptive for men. For example, throughout history rape has been very frequent in wartime, when the possibility of punishment is low. Most victims are in their twenties and 70% of them are between 16 and 35 years old, which seems to indicate that women are selected for rape during their most fertile ages. In addition, the frequency of pregnancy as an outcome of rape is 2% greater than recorded during consensual copulation. Other data indicate that there may be adaptations for rapeavoidance in women. In particular, studies carried out in a range of major cities have found that a high proportion of women develop strategies to reduce the risk of rape. For example they avoid going out alone at night and they avoid the most dangerous parts of town. Moreover, they take greater precautions during their fertile periods. It is also the case that some male rapists are individuals of low socioeconomic status, and are also, although to a lesser extent, unattractive, which means that such men have little success when trying to find a partner in a normal way. Thus, rape in humans is a behaviour that may improve the reproductive success of some males in certain conditions, specially when the costs of rape are low to the rapist. As in other species, including mammals and our closest relatives the primates, rape may be an adaptive strategy. However, attempts at rape have been described in some species in which males attack young, non-breeding individuals who may not even be females. One of the best examples is a study by Christopher Somers and his co-workers of Regina University, Canada, who observed 56 attempted rapes in a colony of American white pelicans (Pelecanus erythrorhynchos) all of which were directed at well grown, feathered chicks whose parents were temporarily absent from the nests. They were especially frequent at a time when there was a spate of late matings within the colony, as a result of which the males were highly motivated to copulate (Somers et al. 2007). Examples such as this also suggest that, at least sometimes, rape may not be the outcome of a reproductive strategy but rather a consequence of the fact that males, which lack access to females, may become so highly sexually aroused that they direct their sexual impulses towards inappropriate individuals. Anyway, even if there exists a genetic predisposition to rape under certain environmental circumstances, this is not to say (as we have already seen in Chapter 1) that rape is either good or morally acceptable. Natural selection, and hence nature, lacks a moral sense. If it did the imperatives of our current society would be very different. For natural selection something `good is any characteristic that leads to increased reproductive success, so that practices such as celibacy, chastity and contraception would be considered bad if natural selection could consider anything, which it cannot. This means that although the existence of genes that predispose men to become rapists may be demonstrated one day, in no way would this discovery provide a justification for the offence. It is undoubtedly the case that our reason and our moral virtues set us apart from all other animal species, as most philosophers have maintained throughout history (see Chapter 1), but this does not mean that we lack instincts, as they suggested, but rather that we must be capable of overcoming them. 46 Chapter 5 Sex, fertilisation, sperm competition and cryptic female choice 5.1. Introduction As we saw in the previous chapter, finding a mate is highly important since failure to do so means failure to reproduce. However, there is much more to it than this. Producing descendants demands successful fertilisation, which is not at all straightforward. Although other types of fertilisation exist (external fertilisation and spermatophore transfer ­ passing a package of sperm), we shall concentrate on internal fertilisation, which is the most interesting in terms of its consequences for animal behaviour. Before and during copulation (see section 5.3) some forms of sexual behaviour take place that serve to stimulate the pair to prepare them for fertilisation. Even once a male has succeeded in depositing his sperm within the genital apparatus of a female he still cannot claim success since many obstacles still remain to be overcome. A second type of sexual selection may occur within the female in which sperm of different males, should they coexist within the female genital apparatus, compete to fertilise the ova (`sperm competition), and the female or her ova may select the most suitable sperm (`selection by cryptic female choice). This chapter considers all these aspects of fertilisation in the order in which they happen. 5.2. Sexual behaviour Not all sexually reproducing species perform sexual antics during the act of fertilisation. Not only does reproduction without sex exist but there is also sex without reproduction, as we humans well know. Among the many claims to exclusivity that we have assigned to ourselves, one of the most often made is that we are `the only animal that has sex for pleasure. In common with many such claims, this one too is false. Plecia nearctica is a dipteran, a member of the order of true flies, known as the lovebug. The males perform courtship displays in flight while flying in a compact group (a lek-type pairing system, see Chapter 6). Females that approach the group to copulate provoke competition between the males as these try to grab a mate. When one succeeds the pair falls to the ground to copulate, a process that in this species ­ hence the name - may last for as long as three days (Thornhill & Alcock 1983). In the prairie vole (Microtus ochrogaster), once a pair is formed, the male and female enter into a frenzy of sexual activity and may remain together copulating frequently for long periods, sometimes for as long as 40 hours (Carter & Getz 1993). The California sea hare (Aplysia californica) is a shell-less marine mollusc. It is hermaphrodite, i.e. each individual has both male and female sexual organs. It has a curious form of reproductive behaviour that perhaps cannot be correctly described as `sex play, particularly since its nervous system is very simple. What is undeniable though is that, to human eyes, what occurs amounts to an orgy of unbridled sex. A detailed study by Steven Pennings, of California University at Santa Barbara, USA, found that, although copulating couples do occur, more often chains of four to eight individuals (sometimes twelve or more) form. In these chains each individual is acting as a male and inseminating the animal in front and, at the same time, is acting as a female and receiving sperm from the individual behind. These copulating chains may persist for days and sometimes for over a week, although the same individuals are not always involved since some leave and others join the chain at times (Pennings 1991). We do not know whether any of the three species described above can be said to `enjoy sex but we can say that they perform sexual behaviour for long periods and sometimes in company, circumstances that are not necessary for achieving fertilisation. Such sexual behaviours have probably evolved on account of their effectiveness, ensuring fertilisation by guarding of the female or through sperm competition (see below). Nevertheless, there are species apart from our own in which the practice of sex that is unrelated to fertilisation has been demonstrated. They include bonobos (Pan paniscus), chimpanzees (Pan troglodytes), other primates such as the white-faced capuchin (Cebus capucinus) as well as various species of dolphins. We shall deal with the sexual behaviour of the first two since I think it will convince even the most sceptical that we are not the only species to practice sex purely for pleasure and without a reproductive purpose. The bonobo, or pygmy chimpanzee, is phylogeneticially very close to the chimpanzee. Both display many similarities in such diverse aspects as morphology, diet, way of life and breeding system (both are promiscuous). However, they are very different in their social organisation (see Chapter 8) and in their sexual behaviour. Regarding the latter, bonobos live in more or less large groups of males, females and juveniles of both sexes. Sexual relations are very frequent within these groups, not only in captivity but also in the wild. We shall summarise the sexual practices of bonobos briefly, mainly following De Waal (1997). The females show genital swelling when in heat but they remain sexually active not only during those fertile periods but also throughout their cycles. Sexual relations are very frequent but, in addition to typical heterosexual copulation, many other sexual practices occur involving all possible sex combinations: male­female, female­ female and male­male. Moreover, it is not just the adults who are involved. Juveniles that have not yet reached sexual maturity also participate. For example, genital contacts between juvenile males and mature females are more common than copulation between adult males and adult females (Hashimoto 1997). Sexual practices include genital contact unrelated to copulation, genital contact using positions similar to those employed in copulation and copulation proper. Actual copulation is most frequent during the females fertile period and the face-to-face `missionary position is not uncommon, despite often being cited as unique to humans. The most frequent sexual contact is genital rubbing between females, which occurs independently of the oestrous 47 cycle. This is not seen in chimpanzees but it is typical of bonobos. Female bonobos have a highly developed clitoris shaped as a half-moon and prominently placed, which no doubt facilitates this behaviour. Genital rubbing between females plays a very important role in social relationships within the group (see Chapter 7), but clitoral stimulation almost certainly produces mutual sexual pleasure, as with other typical sexual practices of bonobos. Sexual relations are very frequent in both bonobos and chimpanzees. In the former both males and females may perform sexual activities as often as thirty times a day. Female chimpanzees are likewise sexually promiscuous but only when in heat. For example, Jane Goodall describes how one such female copulated with eight males in just fifteen minutes and how another that she followed copulated 84 times in eight days with seven different males (Goodall 1986). To conclude, not only are we not the only species to practice sex without having an interest in procreation, but also at least one species, the bonobo, leaves us standing, not only in terms of frequency but also in terms of variety of sexual activity. Another human myth bites the dust. specially developed for the purpose. One of the most curious examples of this latter type of copulation has been described by Nicolaas Michiels, of the Max-Planck Institute in Germany and L. Newman, of Queensland University, Australia, in a study of an hermaphrodite marine flatworm (Pseudoceros bifurcus) that lacks a female genital orifice. Being hermaphrodites, all individuals possess both male and female sex organs but they prefer to perform as males, since the female role involves being penetrated through the body wall, which entails wounding and the risk of infection. When two breeding individuals meet they rear up and engage in a sort of fencing contest with their erect penises, in which each tries to penetrate the other without itself being penetrated. The loser plays the female role in the copulation (Michiels & Newman 1998). 5.4 Sex and copulation in humans: male and female orgasms Some of you may be disappointed but this section is not dedicated to describing the sexual behaviour of human couples. More than enough has been written on that subject in an ever increasing series of publications since Alfred Kinsey published his own studies, on human male sexual behaviour, in 1948, and on that of the human female, in 1953. This is not to say that the subject is irrelevant. On the contrary it is highly important to many aspects associated with mateselection and pair-maintenance. For example, Susan Sprecher, of Illinois State University, USA, has shown that sexual satisfaction during premarital relationships is associated with the degree of love and commitment declared by both members of a couple. There is furthermore a relationship between the degree of that satisfaction and the duration of a relationship, which tends to lasts longer when premarital sexual relations are more satisfactory (Sprecher 2002). This section will only deal with three questions of human sexual behaviour that are important from an evolutionary viewpoint: (1) `Why does sexual desire happen? (2) `Why do we enjoy sex? (with special reference to differences between men and women) and (3) `What do the male and female orgasms signify?. 5.4.1. Why does sexual desire happen? Some months ago, while chatting with some nonbiologist friends, I was told that the reason why sexual desire occurs is obvious. Animals seek mates and copulate because they enjoy it, just as we do. Some species have indeed been shown to show apparent pleasure while having sex but such an answer is not completely satisfactory intellectually since what matters is why the act has evolved to be pleasurable. Why do we enjoy activities that are important for survival, such as eating, or for reproduction, such as having sex, and not scuffing our shins or being in danger? In other words, a satisfactory answer must explain why we enjoy sex but not some other experiences. The ideal is to understand what fires sexual desire and why we enjoy sexual relations. Both of these questions have two types of answers: causal and functional (see Chapter 3). In terms of physiological causes, sexual desire is produced via a complex neuro-hormonal mechanism that is influenced by many factors. In brief, we can say that it arises in the brain on account of testosterone, the 5.3. Copulation In most species with internal fertilisation, males must deposit sperm within the females reproductive apparatus, which they do via copulation. This entails introducing a penetrative organ, or penis, into the females genital orifice, to release sperm within. In most such species, humans included, sperm is deposited in the vagina but in others (e.g. horse, dogs, pigs and their wild relatives) penetration is deeper and sperm is deposited directly within the uterus. Copulation is not always so conventional. In diverse animal groups, such as the platyhelminths (flatworms), leeches, molluscs and insects, there are species in which sperm is injected directly into the female through the body wall. For example, in the bedbug (Cimex lectularius), well-known worldwide as a parasitic feeder on human blood, a male deposits sperm inside the female but not in her genital orifice. Instead he makes a slit in her cuticle using a sickle-shaped appendage at the tip of his abdomen. Once the cuticle has been cut, his penis emerges from a penile groove and releases sperm within the females body. The sperm then swim to find the ovaries where they fertilise the ova (Stutt & Siva-Jothy 2001). Copulation tends to be a collaborative act between both sexes. This is especially necessary in those species that have internal fertilisation but whose males lack a penetrative organ, as in most birds. One of the most common questions that my non-scientific friends and acquaintances ask me is `How do birds copulate if they dont have a penis?. They are surprised by my explanation. Males and females align their cloacas, the common orifice shared by the gut and the genito-urinary apparatus. For a brief period, often less than one second, the female partly protrudes her oviduct. The male deposits his ejaculate on it and, when the oviduct is withdrawn, the sperm is carried into the female. Nevertheless, copulation does not always imply cooperation. The exceptions are not just cases of rape, the absence of cooperation is also conspicuous in species such as the bed bug mentioned above, where the male penetrates the females body wall with an instrument 48 principal driver of sexual desire in both men and women. In women oestrogen too plays an important part, although this hormone does not heighten sexual desire but it makes women more receptive to sex and it is essential for vaginal lubrication. This is one cause for sexual activity, but what then is the functional or adaptive reason for sexual desire? (see Chapter 3). It is the same as we noted in Chapter 4 when studying pair selection and falling in love. Sexual desire is an adaptation that emerges when a suitable mate is found, whether for an enduring relationship or for a casual sexual encounter (see below). 5.4.2. Why do we enjoy sex? The causal answer to the second question is very complex since the neuro-physiological mechanisms involved are not entirely clear and the roles of different hormones are equivocal. In general, according to Panksepp (1998), oxytocin plays the major part and it is responsible for the sensations of affection and satisfaction that are felt during sexual activity. Massive doses of oxytocin are liberated at orgasm and these produce the feelings of tenderness and shared involvement that overwhelm lovers during the period of relaxation that follows moments of intense sexual pleasure. Dopamine (the substance responsible for the pleasure felt by many people when playing or drugtaking) also has an important influence in both men and women, and it drives sex-addiction in some persons. One of the most informative studies on the roles of hormones in sexual relations was carried out by C. Sue Carter, of the University of Maryland, USA, and her coworkers. They studied the prairie vole, the species in which we earlier noted that the male and female copulate very frequently. They found that oxytocin is released during those prolonged bouts of sexual activity and it is responsible for establishing the pairs relationship (Carter & Getz 1993). They also found that in males, pair-bonding and pair-maintenance, which are very strong in this species, depend on the action of vasopressin. They were able to show experimentally that it is this latter hormone that makes a male prefer his own female, even when other females are provided to give him a choice (Winslow et al. 1993). What is the functional or adaptive answer to this second question? As my friends remarked, we enjoy sex and, when all is said and done, those pleasurable feelings increase sexual desire and bring about a higher frequency of copulation. If we consider the scenario in which this behavioural trait evolved in our ancestors, those males and females (men and women) who most enjoyed sex would have had more sexual activity, increasing the possibility of pregnancies. They would thus have left more descendants than those individuals who either did not enjoy sex or enjoyed it less. The offspring of the former would have inherited the capacity to enjoy sex that would thus be passed on to following generations. 5.4.3. What do the male and female orgasms signify? We shall now consider a phenomenon that is intimately related to sexual satisfaction: the orgasm. This topic has given rise to much controversy about whether orgasms occur in primates and other animals, the differences between the male and female orgasm and, above all, the evolutionary explanations for female orgasm. Although sexual pleasure without orgasm exists, the orgasm is the climax of sexual pleasure. It has been defined in a number of different ways but a valid and quite simple definition is: successive waves of pleasure and of tension, increasing in intensity to a climactic point, after which there follows a marvellous sensation of relaxation. The first interesting question is whether or not males and females of other species enjoy orgasms. We can answer this question because orgasm produces a series of observable responses, the main ones being muscular contractions and spasms, a fixed and distracted gaze and a series of specialised and characteristic vocalisations. These signals are sometimes seen in copulating animals and may be interpreted as orgasms. The evidence is clearer in primates given that such orgasms have been seen both during copulation and during masturbation. Manipulation of the genitals by males results in ejaculation and the other symptoms of orgasm mentioned above. The subject has always been more controversial where females are concerned since female orgasm is not accompanied by ejaculation nor by any other easily detectable signal. Nevertheless, it has been noted that in females of various species manipulation of the genital area and the clitoris, either by rubbing against objects or manually, produces indications of orgasm such as an increased heart rate and contractions of the uterus and peri-anal region. One of the studies that most clearly showed the existence of the female orgasm in a non-human species was carried out by Alfonso Troisi and Monica Carosi, of Rome University, Italy, who worked with captive Japanese macaques (Macaca fuscata). They assumed that an orgasm occurred when a copulating female threw her neck backwards and held on to the males fur while undergoing muscle spasms and (sometimes) emitting distinctive cries. After observing 240 copulations, involving 16 males and 26 females, they found that females `enjoyed an orgasm in 33% of cases. The frequency of orgasms was unrelated to the females age or to her dominance rank but was higher when copulation lasted longer. After controlling for duration of copulation and other parameters of physical stimulation, the most striking finding was that orgasms were more frequent when copulation was between a dominant male and a low-ranking female and was less common when high-ranking females were mounted by low-ranking males (Troisi & Carosi 1998). Such studies thus reveal that orgasms are not exclusive to humans and that both male and female orgasms exist in at least some other primates, although apparently (given the behaviour of the sexually active individuals) they are not as intense as those seen in humans. With respect to our own species, comparisons between the male and female orgasm have changed from that promoted by male chauvinists in the past. The female orgasm was formerly considered a by-product of the male orgasm or an imperfect version of it (Sigmund Freud maintained that clitoral orgasm represented an immature state of development in the woman). It is now viewed as a highly intense neuro-physiological phenomenon that is very different from the male orgasm in both its physiological characteristics and in the duration of its various phases. 49 What is the evolutionary explanation for orgasms? The answer is clearer regarding the male orgasm since it is linked with ejaculation and hence with fertilisation. As we said when explaining sexual pleasure, male orgasm promotes the chances of leaving more descendants. Men whose orgasms were most intense would have a greater propensity to copulate and would leave more offspring. However, there is no direct link between fertilisation and the female orgasm. A woman may become pregnant without ever experiencing an orgasm. Moreover, a females orgasm is most closely associated with the clitoris, which receives little stimulation during copulation since it is outside the vagina. Also, no relationship has been shown between frequency of orgasms and numbers of pregnancies or descendants. For these reasons, the female orgasm remains a controversial topic and over a dozen hypotheses have been advanced to explain its existence. The most important of these are included in Box 5.1. 1) Female orgasm plays an important role in pair bonding. It contributes to strengthening the links between a man and a woman in the monogamous long-term pairings that predominate in our species. An orgasm informs a woman of a mans disposition to satisfy her desires and her needs in future. An attentive man who takes trouble to give her sexual satisfaction may be a good candidate for a longterm partner because he would also be disposed to invest his resources in her and her offspring. Female orgasm favours sexual relations with males of higher genotypic quality. This hypothesis emerged when it was found that females were more likely to achieve orgasm with more symmetrical men. Female orgasm increases a mans confidence in his paternity. If a woman is satisfied sexually she will not need to seek such satisfaction with other men. The sexual satisfaction that it produces results in an increased frequency of copulation throughout the whole sexual cycle, leading to a higher probability of pregnancy. The sexual satisfaction that female orgasm produces induces women to have promiscuous sexual relations with diverse men. In a scenario where infanticide is a possibility (see Chapter 1), female orgasm reduces the chances that other males may kill her child later on. The relaxation that follows orgasm causes a female to remain lying down, which reduces sperm loss and so increases the chances of fertilisation. Given the position of the vagina, which is perpendicular to the ground when the woman stands, most of the semen would be lost if a woman got up and started walking immediately after copulation. The vaginal and uterine contractions that occur during orgasm may assist uptake of semen, increasing the chances of fertilisation. 2) 3) 4) 5) 6) 7) 8) Box 5.1. Different adaptive explanations for the human female orgasm. As can be seen, some of the hypotheses are contradictory. Many are supported by some particular study but the methodology of some of these investigations leaves much to be desired and has often been criticised. Which of these hypotheses are most convincing? Answering this question is not at all straightforward and certainly several of the ideas proposed have a more or less significant role in the evolution of the human female orgasm. To allow you to draw your own conclusions, we shall summarise some of the most important findings of a variety of studies based on interviewing women. The information given here is drawn from several sources but chiefly from Buss (2007): (1) Female orgasm is more frequent when sexual relations occur in the context of a stable, long-term relationship. Married women or those with a steady partner have more orgasms than unmarried ones or those without a steady partner. This is quite a reliable result since it has emerged in various studies in different parts of the world. (2) Women in a stable relationship who enjoy a higher number of orgasms claim to be happier with their marriage or relationship than those who have fewer orgasms. (3) Women who experience fewer orgasms say that they are more eager to have sexual relations with other men than do women who enjoy orgasms more frequently. (4) Women whose partners are more attractive and more symmetrical (indicators of higher genetic quality, see Chapter 4) say that they have more orgasms than do women paired with less attractive and less symmetrical men. (5) Women in stable relationships who have extramarital affairs are more than twice as likely to achieve orgasm with their lovers than with their husbands. This is also quite a reliable result that has been confirmed in a diversity of studies, perhaps because women are very selective about having extramarital affairs with men of high quality (see below). The matter of female orgasm remains an evolutionary enigma that we are far from solving, especially when we consider two further problems to which we have not yet referred. Firstly, the frequency of orgasms differs greatly between cultures, orgasms are quite common in some and practically unknown in others (at any rate according to information gathered in interviews by anthropologists, which is not always reliable). Secondly, adaptationist theory predicts that, if the female orgasm is an adaptation, the male should have developed strategies to exploit it. For example, he should be keen to ensure that his partner reached orgasm, he should ejaculate at the same time or just after she did so, or he should have developed a capacity to detect the female orgasm so that the female could no easily fake it. The first of these predictions is only sometimes fulfilled, given that only some men are concerned about promoting orgasm in their partners, but the other two predictions are rarely met. We have seen that orgasms also occur in other animals, at least in some primate species. Why however are orgasms more intense in humans? I wish to suggest a reason that seems quite plausible to me: it has developed as an evolutionary response to human resistance to conception. We know that diverse contraceptive methods have been developed by all people and all cultures, given that conception is costly (especially in particular circumstances such as when food is short or another small child is still being raised). Human intelligence has been used to avoid pregnancy especially by abstinence from sex and by withdrawal prior to ejaculation. This would engender significant selective pressures that may have favoured the development of more powerful orgasms, given that a higher degree of sexual satisfaction would encourage hasty and unintended encounters that would reduce the effectiveness of conscientiously employed contraceptive measures. Despite the latter, individuals with more intense orgasms would leave more descendants. 5.5 Male/female conflict in sexual relations Conflict between the sexes is a significant phenomenon. The most widespread aspect, which has been detected in most species, relates to avoiding extra-pair mating. The motives vary a great deal according to species but in general it is not in the interest of a male for his female to copulate with other males and similarly is not in the interest of a female for her male to copulate with other females. We shall consider the sperm competition that is 50 associated with extra-pair mating in the next section. Here we focus on conflict associated with the frequency of sexual relations. This type of sexual conflict is very common in humans and quite rare in other animals but an example from the insects illustrates it perfectly. I speak of waterstriders, aquatic hemipteran insects that walk on water surfaces. As a result of the conflict between a male and a female about when to copulate and for how long, males have developed structures for grasping females and females have developed structures to prevent males from capturing them and to make escape from grasping males more easy. In these insects, as with most other species, males are nearly always ready to copulate (see Chapter 4). They try to seize a female with their front legs and climb onto her back in order to mate. Furthermore, they try to remain on the female as long as possible since this increases the chances that their sperm will fertilize her eggs. Such pairings are costly to females since they increase the risks of predation considerably. Thus a significant conflict exists between the sexes. Göran Arnqvist, of Uppsala University, Sweden, and Locke Rowe, of Toronto University, Canada, have shown in a study of fifteen water-strider species that both males and females have developed morphological structures for use during pairing. Males have a specialised structure within their genital apparatus for attaching to females, but females have developed abdominal spines that may be pushed downwards to interrupt copulation. Strong evidence regarding the function of these structures comes from Arnqvist and Rowes comparative study, which showed that the more highly developed the males attachment structures were, the more highly developed the females anti-male spines. This is a clear demonstration that these structures have evolved in both sexes as a result of a coevolutionary arms race (see Chapter 9) between males and females for control of copulation (Arnqvist & Rowe 2002). In human beings, as in water-striders, there also exists an important inter-sexual conflict regarding the number and duration of sexual relations, once a pair is established. In all interview-based studies, men complain that they have less sex than they would like, a finding that is repeated across all cultures. Men think about sex much more often than women do and are always more disposed than women to feel sexual desire and to indulge in sexual activity (see Chapter 4). This should come as no surprise to anybody since men not only have much higher blood testosterone levels than women (ten to 100 times higher) but also the neural centres associated with sexual activity in the male brain, located in the hypothalamus, are twice the size of those in the female brain. In contrast, women think about sex less often than men do and they tend to be much more sentimental and emotional. The prefrontal cortex, the cerebral structure that is responsible for emotions, is much more highly developed in the female brain than in that of the male (Brizendine 2006). These physiological differences may explain the fact that men and women have different preoccupations when it comes to their feelings about their relationships. A woman is little affected when the frequency of sexual activity declines but a man will be very concerned and will think that his woman no longer loves him or has taken a lover. However, the opposite happens if communication and signs of affection decline between the man and his partner, in which case the woman tends to conclude that her mate no longer loves her. As promoters of pair stability, sex is most important to a man but to a woman what matters most is feeling loved, getting a lot of consideration and not having to worry. More than this, if such conditions are not met a woman may come to lose all interest in sex. Although the reality may seem harsh, available data suggest that a woman offers affection and sex in exchange for love, whereas a man offers affection and love for sex. Of course, we are talking about general `rules, statistical averages in behaviour, for which there will always be lots of exceptions. I think it quite probable that a coevolutionary arms race, as has occurred with the water-striders, may also have happened with human females ­ of course in an entirely unconscious manner given that we are speaking of evolutionary strategies. Bearing in mind that women tend to lose sexual interest when in unsatisfactory relationships, they may have succeeded in obtaining benefits, such as additional resources for the family or more care for the young, in exchange for providing greater sexual pleasure for a partner. Anyone reading these lines may well conclude that I am a highly unromantic person. This is not so. Rather, I use an evolutionary approach because it allows us to understand the biological basis of conflict behaviour, which might even help us to resolve relationship problems in our daily lives. Just this once I am going to play the part of a sex counsellor and say that many relationship breakdowns would be avoided if both parties were aware that most such problems derive from the differences between men and women described above. These differences can generate a vicious circle in which a reduction in the frequency of sexual relations cannot be solved without increased communication and demonstrations of affection, which will not occur without an increase in sexual activity. 5.6. Male and female genitalia Males of those species in which fertilisation is internal require an intromittent organ to release their sperm within the females genital apparatus. This structure, the penis, is extremely variable among species, not just in size and shape but also in how it is employed. Some species with internal fertilisation lack a penis, as is true for most birds. Nevertheless, some birds do have a penis and some, such as ostriches, swans and ducks, have one of considerable size. An extreme case is the Argentine blue-bill (Oxyura vittata), a small duck in which males have a penis 20cm in length (McCracken 2000). Although males with penises typically have just one, some male lizards and snakes have two penises, and certain marine platyhelminths have more than a dozen! The shape of the penis varies from species to species. In most cases, the device resembles a tub, but it may be corkscrew-shaped, as in domestic and wild pigs, or blade-shaped, as in certain squirrels. In addition, it may be accompanied by a great variety of structures including lumps, filaments, spines, hooks or even, as in most primates, a bone. Penis size is also very variable. Some barnacles (hermaphrodite crustaceans that live permanently attached to their substrate) have penises that may be two or three times the length of their owners bodies, allowing them to reach and fertilise neighbouring 51 individuals. They are, however, not the record holders in terms of penis size since some slugs have extremely long penises. The champion in this respect is surely Limax redii whose body is some 12cm long but which has a penis longer than 80cm (Birkhead 2007), i.e. seven times longer than its body! What about primates? As a general rule, male primates have small penises that are kept permanently rigid thanks to the presence of the penis bone or baculum. This is not the case in our own species, not only in that the human penis lacks a baculum, but also because it is relatively large. The erect human penis is some 15cm long, whereas that of the chimpanzee and bonobo is 7cm long, the orangutan penis measures 4cm and the mighty gorilla has a penis only 3cm long. Such great variation between species in both the shape and size of the penis had led some evolutionary biologists to suggest that it may have other important functions apart from inserting sperm in the female genital apparatus (see below). The female genital apparatus also varies according to species, which is to be expected since in order for copulation to be possible the penis must be adapted to penetrate the female orifice and the latter must be adapted to receive the penis of males of the same species. This much refers to the vagina but other, external, structures of the female genital apparatus are also very varied where they exist. For example, among anthropoids, female chimpanzees have a very long, straight clitoris, female bonobos also have a large clitoris but shaped like a half-moon and human females have quite a small clitoris that is some distance from the vagina. The clitoris is also very variable among other primates. In many lemur species and also in spider monkeys (American monkeys of the subfamily Atelinae), the females have enormous, pendulous clitorises. Zoologists have known for centuries that the genital organs differ greatly among species, so much so that, in many groups of insects and other invertebrates, precise identification of individuals of closely related species is only possible by removing and examining their genitalia. Species that are so similar as to be inseparable on the basis of external morphology often possess different genitalia that allow them to be correctly and speedily identified. Why should this be? The evolutionary explanation is quite clear. The selective pressures that favour both those males who are effective at fertilising females and those females who succeed in being fertilised by the best males are so strong that they bring about rapid evolutionary change of their genitalia that gives rise to new species (divergence) that differ in their genital morphology. Göran Arnqvist, the Swedish investigator to whom we referred earlier in this chapter, carried out a comparative study of the genital apparatus and external morphology of insects. In accordance with what we have just said, he found that divergence between species was much greater in terms of genital morphology than with respect to all other morphological characters (Arnqvist 1998). These findings strongly support the idea that sexual selection (see Chapter 4) acts on the genitalia of different species in a direct manner. In the same way, among primates it has been found that males of species with promiscuous females have longer and more complex penises than do males of monogamous or polygynous species (Dixson 1987). To return to the human penis, why should our species have evolved such a large penis relative to that of the other primates? There is no clear answer to this question although various hypotheses have been advanced. For example, it may be a visible signal that can be employed in sexual selection or it may increase the chances of women achieving orgasms. One of the most accepted ideas is that a longer penis is an aid to fertilisation since it deposits semen closer to the ova. The key question with respect to all that we have dealt with in this section is `Why is there so much variability in penile structures? Two hypotheses attempt to answer this: the `lock-and-key hypothesis and the `sexual selection hypothesis. The former suggests that the high degree of variation is because the precise match of the penis to the female genital orifice prevents interspecific mating, which would amount to a great loss of time and energy since hybrid matings rarely produce viable offspring. The sexual selection hypothesis suggests that the evolution of both the male and the female sexual apparatus is governed by two powerful influences that we studied in the previous chapter: competition by males and female choice, only that this time they operate within the females body (see below). The lock-and-key hypothesis is the older of the two and is the choice of classical zoology, but the sexual selection hypothesis has received powerful support more recently, in particular Göran Arnqvists comparative study of insects (Arnqvist 1998), which tested some of the predictions that arise from each hypothesis. One prediction is that since the lock-and-key hypothesis is thought to prevent errors in species-choice when mating, it would be expected that monogamous species, in which females only mate with one male so that mistakes would be disastrous, would have the most complex genitalia. In contrast, the sexual selection hypothesis predicts that greater male genital complexity would be found in polyandrous species. In these a female mates with several males and competition between the sperm of these (selection by sperm competition among males) and any choice the female may make of the most adequate sperm (selection by cryptic female choice) are the decisive factors. Both these concepts are studied in detail below. Arnqvist analysed the morphological complexity of the genitalia and other characters in monogamous and polyandrous insect species. He found no significant differences between these two groups in morphological characters other than in the genitalia, where the differences were very clear. The genitalia of males of polyandrous species were almost always much more complex than in males of monogamous species (Arnqvist 1998). These results amount to resounding support for the sexual selection theory as opposed to the lock-and-key hypothesis. 5.7. Sperm competition In the early 1970s Geoffrey A. Parker made a fascinating scientific contribution when he proved that competition between males does not end with copulation but instead, that when a males ejaculate coexists with that of another male within the female genital tract, competition to fertilise the ova continues between the sperm. This phenomenon is termed sperm competition and the discovery introduced a revolution in the field of reproductive biology. A multitude of studies have since 52 revealed that sperm competition is a very significant and widespread force in evolution. Molecular studies of paternity have revealed that females often copulate with more than one male during the same fertile period. This even happens in species, such as birds, which have previously been considered to be monogamous, a realisation that has made it necessary to distinguish between social monogamy and genetic monogamy. By definition, monogamous species are those in which a male and a female form a pair, that is to say, an association that endures throughout the breeding season. Nevertheless, genetic monogamy, in which all the offspring are those of the male and the female that comprise the pair, is very rare. This is because, as we have noted, females very frequently copulate on the side with additional males, so that some of their offspring are not those of the `social father. Since males may increase their reproductive success considerably by inseminating a larger number of females (as mentioned in Chapter 4), it is unsurprising that males court females who are already paired in order to obtain extra-pair copulations. A spectacular example involves a small, beautifully coloured Australian bird, the superb fairy-wren (Malurus cyaneus). In this species a male and a female form a long-standing relationship that may endure for several breeding seasons. Nonetheless, a very high percentage of nests include a chick that is not the offspring of the incumbent male. Raoul Mulder, of Melbourne University, Australia, studied male behaviour and, remarkably, he found that when a male courts a female who is not his own mate he employs a different approach. After finding a female in a neighbouring territory, he presents her with a petal or a flower (Mulder 1997). On 97% of occasions when this behaviour was seen the male was courting a female that was not his. The `wife never gets any flowers! Since males have most to gain from extra-pair copulations there has been a widespread belief that it is they that are principally responsible for initiating them. However, many observers feel that females do not just accept extra-pair copulations but actively seek them. Probably the most conclusive study of this is by Bart Kempenaers and his coworkers of Anwerp University, Belgium, who made detailed observations of the behaviour of male and female blue tits (Cyanistes caeruleus) during the fertile periods of the latter. They found that it was the females who chose males that they preferred for extra-pair copulations (Kempenaers et al. 1992). If females actively seek out such copulations with other males, what benefits do they derive? As we pointed out in Chapter 4, a female cannot increase the number of chicks that she raises by increasing the number of males that she mates with, but by doing so she might increase the quality of her offspring. This is the principal hypothesis explaining extra-pair copulations: females choose the best available males to achieve offspring of higher genetic quality. Another study of blue tits by Bart Kempenaers and his team provides a good example. When they examined instances of extra-pair paternity they found that 11­14% of chicks were not offspring of the male nest-owner and paternity due to other males affected a high proportion of nests (31­47%). Paternity was established by means of highly reliable molecular analyses. They found that the most successful males, those whose nests contained only their own young but who also had fathered some young in other nests, had larger tarsi, sang longer song phrases and also survived better. Chicks who were the outcome of extra-pair copulations tended to be males and survived better than those fathered by the nest owners (Kempenaers et al. 1997). Such data thus supports the idea that females paired with males of lower biological quality seek extra-pair copulations with better males, which allows them to improve the quality of certain of their offspring. Such extra-pair copulations are responsible for many socially monogamous species being polyandrous from a genetic viewpoint (all the young belong to the mother but they are the product of several fathers). These findings make clear that sperm competition imposes very strong selective pressures. Males must be effective not only at securing mates but also at ensuring that it is their sperm that fertilises the eggs of those females. As a result of such selective pressures males have evolved a large array of adaptations, behavioural as well as structural, to reduce the chances that the sperm of another male may fertilise the eggs and to increase the chances that it is their own sperm which succeeds. We shall consider these adaptations by classifying them according to the advantages that they confer (see Box 5.2). 1. PREVENTING THE FEMALE FROM COPULATING WITH ANOTHER MALE a. Female guarding: In most species this involves the male remaining by the female after copulation, so delaying any possible copulation by another male. b. Blocking the females genital orifice: Along with the ejaculate, males of many species inject a sticky substance that forms a stopper closing the females genital orifice after copulation. c. Preventing the female from being attractive to other males: This is infrequent (see text). d. Inhibition of female sexuality: The male ejaculates of some insect species contain anti-aphrodisiacal substances that reduce the propensity of the females to copulate again. 2. PREVENTING SPERM PREVIOUSLY INTRODUCED BY OTHER MALES FROM FERTILISING THE EGGS a. Increasing copulation frequency: This is entirely a behavioural adaptation. Copulation is much more frequent in species in which a female cannot be guarded effectively and in which extra-pair copulations are common. b. Increasing the sperm density of the ejaculate: In many species exposed to high levels of sperm competition, the testes are larger and produce more copious ejaculates, containing a larger number of sperm. c. Removing semen that has been previously inoculated by another male. In many insect species the male genital apparatus includes structures that are used to remove semen stored within the female genital tract. 3. TAKING ADVANTAGE OF WORK DONE PREVIOUSLY BY OTHER MALES (see text) Box 5.2. The principal sperm-competition strategies employed by males of different species 5.7.1. Preventing the female from copulating with another male Once a male has succeeded in being accepted by a female and in copulating with her, any strategy that may contribute to reducing the chances that she can mate with another male could be adaptive, since then his sperm will not have to compete with that of others to fertilise the eggs. Four types of such strategies may be distinguished (Box 5.2 - 1), and we shall now consider them in turn. Mate guarding is quite frequent in birds and in insects and other arthropods. Before the discovery of sperm competition, the frequent observations of male 53 birds remaining close to their females were regarded as a way of strengthening the pair-bond. We now know that the motive is less romantic. The male stays close to his female to prevent her from copulating with other males. More drastic evolutionary strategies have evolved in cases where the males do rather more than merely staying close to their females. For example, many male insects tend to remain on top of the female for some time after copulation has ended. For example, in many dragonflies and damselflies such as the azure damselfly (Coenagrion puella), the male guards the female until she has laid her eggs, and he does it by holding her thorax with a pincer at the tip of his abdomen. This strategy is costly for the females since it renders them less mobile and so more vulnerable to predation. Females have thus tended to develop mechanisms for ridding themselves of males and the latter have developed counter-adaptations that allow them to remain attached for longer. Surely one of the most extreme strategies evolved by males to guard their females is seen in canids, both wild and domestic. The male and female remain attached after copulation by the swelling of the penis, which does not allow them to disengage. This is a highly effective mate guarding strategy. Since the female cannot copulate again until the pair separates, it gives the males sperm an advantage over that of his rivals and increases his chances of fertilizing her eggs. The advantages of mate guarding have been analyzed in some studies. For example, Helen ChuangDobbs, of New York State University and her coworkers performed an observational and experimental study of a small bird, the black-throated blue warbler (Dendroica caerulescens), in which molecular techniques were used to establish paternity of all chicks. They found that males who guarded their females most closely had less chance of having chicks fathered by others in their nests. Also, when a male was removed and kept isolated from his female for an hour, there was an increased chance that one of the chicks in his nest was fathered by another male (Chuang-Dobbs et al. 2001). Another effective strategy for preventing a female from mating with another male is to block her genital orifice. This tactic has been described from a wide range of animal groups, including worms, spiders, insects, snakes, rodents and bats. On the face of it, such a `chastity-belt would seem to be a very effective way of stopping another male from mating with a female. However, it is not always so. As a result of the evolutionary mechanisms of sperm competition, males of many species have developed ways, and even structures, that allow them to remove the plug from a females genital orifice. Some species have evolved a truly dramatic way of producing the genital stopper. For example, in the European honey bee Apis mellifera, once a drone has finished copulating with the queen he explosively fire his genital apparatus into the females genital opening, which plugs her orifice (Gary 1963). This action kills him but no matter because he has achieved his objective of inseminating her and in this way he is increasing the chances that it will be his sperm that fertilised her eggs. Another convoluted and Machiavellian way of making use of the genital plug has been found in males of the spiny-headed worm Moniliformis dubius, an acanthocephalan intestinal parasite of rats. In this species, as in many others, the males sperm forms a plug at the entrance to the females genital orifice. What is unusual is that dominant males sometimes `copulate with rival males and seal their genital orifices in the same way, preventing them from transferring sperm to females (Abele & Gilchrist 1977). As we indicated in Box 5.2, another mechanism for avoiding insemination of a female by other males is to ensure, after copulation, that she becomes unattractive to them. This is uncommon since it is not easy to achieve (except in humans, see below) but a good example is provided by the butterfly Heliconius erato. Gilbert (1976) found that females smelt oddly after copulation. He later found that it was not the female who produced a malodorous substance. The male deposits it during copulation and this serves as a powerful counteraphrodisiac against even the most determined males. Another possibly way of avoiding copulation between a female and another male is to inhibit her receptiveness. This too is uncommon but in some insects it has been shown that the males ejaculate contains antiaphrodisiacal substances that reduce the females disposition to copulate. A well known case involves the housefly (Musca domestica). Rieman et al. (1967) showed that a substance transferred with the sperm not only delayed searching for new males by females, but quite often led to females not copulating again for the rest of their lives. 5.7.2. Preventing sperm previously inoculated by other males from fertilising the eggs Despite the adaptations described above, males often cannot prevent a mate from mating again with another male. Where there is a high chance that other males have copulated previously with a given female, natural selection favours those individuals that develop mechanisms that prevent or reduce the likelihood that previous ejaculates fertilise the eggs. A wide range of strategies to achieve this adaptive goal exists in nature. One way in which a male can succeed is to ensure that his sperm are in the majority within the females genital apparatus, simply because this increases the odds that some of his sperm will fertilise the eggs. This result can be achieved either by increasing the numbers of a males sperm present or by removing those previously introduced by other males (see Box 5.2). Another obvious fertilization tactic is to increase copulation frequency. Many examples demonstrate that copulations are very frequent in those species in which a female habitually mates with several males. This is also the case in those where a female cannot be guarded effectively, as happens with raptors and seabirds, where one member of the pair remains to guard the nest while the other seeks food. One such species is the goshawk (Accipiter gentilis). The male cannot guard the female and copulation correspondingly occurs very frequently. According to a study by Anders Møller, then at Aarhus University, Denmark, goshawks copulate astonishingly often for an average of 518 times per clutch. Many of these copulations take place when the male returns from a foraging trip to the nest. Males copulated within 30 minutes of their return on 20 out of 52 occasions and did so, on average, after 72.8 minutes (Møller 1987). The high frequency of copulations on return in species in which the male cannot guard his female effectively 54 offers evidence of the close relationship between high copulation frequency and sperm competition arising from extra-pair copulations. Another mechanism that may confer a sperm competition advantage is to produce ejaculates with a high sperm density. Under conditions of sperm competition, the greater the number of sperm transferred by a male, the higher the chances that the offspring will be his. Numerous studies have established that the greater the level of female promiscuity, the larger the testes and the larger the number of sperm produced by the males. Nevertheless, following a rule of `transferring the maximum possible number of sperm is not always adaptive because although sperm are cheap to produce their cost is not negligible. The rate of sperm production is limited in males of all species. It may thus be predicted that the number of sperm transferred would be adjusted according to the reproductive benefits that a male can obtain on each occasion, at least in species in which copulations are frequent. A series of fine studies by Tim Birkhead of Sheffield University, UK, and his co-investigators have shown that at each copulation domestic fowl cockerels (Gallus gallus domesticus) transfer a variable number of sperm to hens, the quantity depending as much on the males status as on the females quality and her level of promiscuity. Dominant cocks, which have preferential access to hens, adjust the quantity of sperm transferred according to the number of hens in their flock. On the other hand, subordinate cocks, whose copulatory activity is restricted by the dominant males, always transfer a high number of sperm (Cornwallis & Birkhead 2006). Both dominant and subordinate males reduce the number of sperm transferred to a given hen in successive copulations but, nevertheless, if they are then presented with a new hen they are capable of increasing the sperm density of their ejaculate immediately (Pizzari et al. 2003). Female quality is another factor that influences the quantity of sperm ejaculated significantly, in accordance with the idea that sperm donations are adjusted in relation to the benefits associated with the males investment. Males ejaculate a larger quantity of sperm into higher quality females, namely those whose secondary sexual characteristics are more developed, since these hens are the ones that most invest in caring for the chicks (Pizzari et al. 2003). Another strategy that would be very effective if possible would be to remove sperm that another male has previously inseminated (see Box 5.2.). A very large number of mechanisms evolved for this purpose have been described, especially in insects. Krebs and Davies (1993) give two highly instructive examples involving dragonflies, which we will now consider. Males of the black-tailed skimmer (Orthetrum cancellatum) have a structure consisting of a dense group of filaments that they insert into the females genital orifice before beginning to transfer their sperm. When they withdraw the filaments these are laden with any sperm that other males may have inserted earlier. Males of the scarlet darter (Crocothemis erythraea) possess a type of `inflatable horn that they insert into the female and that, once inflated, displaces any stored sperm to the sides or to the exterior. A fascinating example of sperm competition involving sperm withdrawal has been reported in a small bird, the dunnock (Prunella modularis). Females in this species are highly promiscuous (see Chapter 6) and males have developed a famous behavioural adaptation in response. Nick Davies, of Cambridge University, UK, noted that the males peck at the females cloaca before copulating. He showed that this induces the female to expel sperm inserted during earlier copulations with other males (Davies 1983). 5.7.3. Taking advantage of work done previously by other males We have now seen some truly surprising adaptations resulting from sperm competition. In this section we shall consider two further remarkable examples, the second of which borders on the incredible. Fertilisation in many tailed amphibians (urodeles) is via a spermatophore that the male deposits on the ground after courtship. He then has to ensure that the female lowers her cloaca on to it and presses down until the spermatophore passes into her body. Sperm competition arises in the spotted salamander (Ambystoma maculatum) since some males (satellite males, see below) watch those that are courting and, when these have dropped their spermatophores, the rival males deposit their own spermatophores on top. Thus when the female lowers her cloaca she takes in not the spermatophore of the male that courted her, but that of the opportunistic satellite male (Arnold 1976). We have already seen how fertilisation in some species does not occur via the female genital opening but through the body wall, within which sperm are liberated to swim freely to reach the ova and fertilise them. In the cave bat bug (Xylocoris maculipennis), a hemipteran insect, dominant males may behave in this way not only with fertile females but also with males weaker than themselves. In the latter case, sperm from the dominant male swim to the testes of the subordinate males and enter within. In this way, when a `raped male mates with a female, he also introduces the sperm of the dominant male (cited by Krebs & Davies 1993). 5.7.4. Human sperm competition As a general rule, we humans belong to a species in which one male and one female form an enduring relationship within which children are born and raised. These circumstances are very like those seen in most birds, a group in which there is often a predisposition to extra-pair copulations and hence to sperm competition. The intensity of sperm competition in humans is controversial since experts disagree. Without going into detail, we shall simply quote some figures. For one thing, studies on conjugal infidelity in different populations have found that 40­50% of men and 18­ 26% of women have had at least one extra-pair sexual adventure. In addition, paternity studies have revealed that the social father is not the genetic parent in a variable percentage of cases, ranging from 1­30% among populations with a mean of 10% of children (Buss 2007). Nevertheless, not all of the studies on conjugal infidelity and paternity reviewed by Buss employed reliable methodology. According to Simmons et al. (2004), if only the most rigorous studies are included, the mean percentage of people who have had extra-pair relationships varies from 2­27%, and extrapair paternity is approximately only 2%. Whereas the data in Buss (2007) imply the existence of strong sperm 55 competition, those presented by Simmons et al. (2004) suggest that such competition is quite limited. In short, the argument goes on. Criticisms of those who maintain that a high level of sperm competition exists in humans are well founded since some studies of the subject are not highly rigorous. Indeed, the famous results obtained by Baker & Bellis have not been repeated by others using the same methodology. Nevertheless, sperm competition in humans may be greater than critics maintain, for two reasons. Firstly, in hunter-gatherer communities, where effective modern contraceptive methods are not used, quite a few children are said not to belong to their `official fathers (about 10% according to the most conservative data in Simmons et al. (2004)). This suggests that sperm competition may well have been considerable during our evolutionary history. Also, if this is so, both men and women would be expected to possess adaptations related to sperm competition. The second reason why I believe that such competition is, or at any rate has been, more intense than some critics suggest has to do with the many physiological and psychological attributes of men and women that only make biological sense in the light of sperm competition. We shall consider them in the next two sections. Another important fact supports my conclusion, the relative size of the testes in relation to male body size in our species. It is well known from a wide range of animals (insects, fish, reptiles, birds and mammals) that relative testis size is a good indicator of the intensity of sperm competition. Males in which such competition is intense have larger testes, enabling them to produce more sperm, than those in which there is little sperm competition. A. H. Harcourt of Cambridge University, UK, and his co-workers conducted a comparative study of testis size in primates. They found that males of species in which females are promiscuous and copulate with all the males in the group (which are therefore exposed to strong sperm competition) have significantly larger testes in relation to body size than do males of monogamous species (where one male pairs with one female) or polygynous ones (where one male pairs with several females). In a graph of relative testis size in the genera studied, Homo falls between the chimpanzee, in which males and females live in groups, and the gorilla, in which one male controls several females, which are unlikely to engage in extra-pair copulation (Harcourt et al. 1981). This finding supports the idea that sperm competition exists in our species, although to a moderate extent, and that the typical human pairing arrangement would comprise a male paired with one female with only a modest risk of extra-pair copulation occurring (see Chapter 6). 5.7.4.1. Biological and psychological adaptations to sperm competition in humans The most important of these are given in Box 5.3, separately for men and women. With respect to human beings, in many cultures the man makes a sizeable investment by providing the necessary resources for raising the children. It is a very costly business for a man if his woman is impregnated by another man since, from an evolutionary point of view, his investment is wasted since it does not contribute to perpetuating his genes. Natural selection may therefore be assumed to have favoured strategies that are more effective in preventing other men from fertilising ones partner. We need therefore not be surprised by the great diversity of `anti-cuckold strategies, both biological and cultural, which have been developed by human males. In men we can find nearly all the behavioural mechanisms of sperm competition that we earlier described for animals in general, those listed in Box 5.2. As in many species, female guarding is widespread and takes many forms (see also the next section, on cultural `adaptations). In addition, some findings indicate more subtle mate guarding. For example, a man guards his partner more carefully when there is a greater risk that an extra-pair copulation may produce a pregnancy, i.e. when his wife is young and not pregnant (see Box 5.3a). Other adaptations that were described for animals in general and that are also seen in the human species when the risk of extra-pair copulation is high include increasing copulation frequency and increasing the sperm concentration of the ejaculate (Points 3, 4 & 5 in Box 5.3a). a) Adaptations in men 1. Guarding of mates is widespread in men. 2. Men guard their partners more closely when these are young and not pregnant than when they are older or pregnant. 3. Men increase the frequency of copulation when there is a greater risk of extra-pair copulation. 4. The longer a man is separated from his partner since their last copulation, the more attractive she becomes to him and the greater his desire to have sexual relations with her. 5. A greater number of sperm is transferred per ejaculation in relation to the length of the period that a man is separated from his woman since their last copulation. 6. Some authors have interpreted the shape of the human penis as an adaptation for displacing sperm deposited by another man during an earlier mating. 7. A man who suspects infidelity exacts significant costs from his partner, such as physical and psychological abuse, rape and divorce. 8. Men find the odour of women more agreeable when these are in their fertile period. 9. Men guard their partners more closely during their fertile periods than during the rest of the menstrual cycle. 10. Men are more attentive and more possessive towards their women during their fertile period. b) Adaptations in women 1. Women select more attractive and more symmetrical men (with good genes) for casual sexual relations. 2. Women in stable relationships who have extramarital sexual relations are more than twice as likely to have orgasms and to become pregnant with their lovers than with their husbands. 3. A womans interest in her partner does not increase during her fertile period but her attraction to other men does so. 4. During their fertile periods women find the odour of more symmetrical males more attractive. 5. During their fertile periods women find males with more masculine faces (indicating higher testosterone levels) more attractive than at other times. 6. During their fertile periods women prefer men whose actual or potential genetic quality is greater than that of their partner. 7. During their fertile periods women prefer men who appear more confident and competitive in the presence of other men. 8. During their fertile periods women alter their behaviour to reduce the risk of rape and thus of impregnation by an undesired male. c) General adaptations of both sexes 1. Pair disruption strategies 2. Pair maintenance strategies: courtship Box 5.3. Adaptations of men and women that support the existence of sperm competition. From various sources but chiefly after Gangestad et al. (2002) and Shackelford & Pound (2006). There has also been an attempt to explain the shape of the human penis as a tool to withdraw sperm deposited by other males during recent copulations. We have noted how anatomical adaptations have quite frequently evolved for this purpose in different animal groups but 56 no attention was given to this matter in relation to human males until Gordon Gallup, of New York State University, and his co-workers, performed an investigation. They used liquids to simulate semen of different densities and artificial vaginas and penises, such as may be obtained from sex shops. They were able to demonstrate that the shape of the human penis, in particular the widening at the base of the glans, makes it quite effective at withdrawing sperm that has previously been deposited in the vagina (Gallup et al. 2003). In most species, males and females maintain sexual relations only during the breeding season, when the females are fertile. In humans, in contrast, women are potentially sexually receptive at all times. Thus, since extra-pair copulations by the woman are only costly for her man during the fertile period, selection will have favoured adaptations that enable mate guarding during that fertile period, which takes up about seven days each month (from the 7th to the 14th day of the menstrual cycle). As seen in Box 5.3a, that prediction is fulfilled. Men find their wives more attractive and find their odour more agreeable during the fertile period than at other stages of the menstrual cycle, and they guard them more intensely and behave more attentively and possessively towards them at this time (Points 8, 9 & 10 in Box 5.3a). Two adaptations associated with long-term and short-term pair selection have been detected in women. We considered these in Chapter 4 and they comprise points 1 and 2 in Box 5.3b. There are also other adaptations that refer to changes in behaviour or strategy according to whether or not a woman is in her fertile period or at another stage of the menstrual cycle (points 3­7 in Box 5.3b). In particular, her attraction to other men increases during her fertile period, when she also finds the odour of more symmetrical men and those with more masculine faces more alluring as well as preferring men who show themselves to be more self-assured and competitive in the presence of other men. All these tendencies show that during the fertile period women prefer mates whose actual or potential genetic quality is high, as occurs with female blue tits, something that does not occur at other stages of the menstrual cycle. It is curious to see that these changes arise only with respect to casual sexual relations and no significant trends arise when a woman is selecting a long-term partner. This data on changes in preference during the fertile period support the idea that women are particularly predisposed to selective extra-pair matings at that time, which leads to sperm competition. These changes allow women to obtain genetic benefits by means of extra-pair copulations. This is not surprising because, at least during most of our evolutionary history as hunter-gatherers, most women will have been paired with men of medium or low genetic quality. They could therefore obtain significant genetic benefits for their offspring by having occasional sexual relations with men of high genetic quality. Nowadays, at least in our industrialised western societies, this tendency may be concealed by the widespread use of effective contraception. The drive to produce better quality children through copulating with men of higher genetic quality would not have involved a conscious decision (any more than it is among female blue tits). It would be the outcome of evolved psychological mechanisms. A preference for such men during the fertile period may endure in modern societies but very often the women employ contraception, even more carefully than when having sexual relations with their regular partners, because of the risk of pregnancy or of acquiring a sexually transmitted disease. The use of contraceptive methods clearly amounts to a behavioural revolution that will do away with current adaptations and may eventually lead to the development of new ones. This though is another matter and many generations must pass before we can know what transpires. I do not want to end this topic without making one point clear. The changes mentioned in relation to the womans fertile period do not mean that she has a general interest for men other than her husband during this time. What happens is that when such an interest arises it is highly selective so that women tend to be attracted to men who display signs of high genetic quality. With respect to adaptations common to both sexes, Box 5.3 notes the tendency of some to disrupt established pairs in order to acquire a partner and the role of jealousy. David Schmitt, of Bradley University, USA, and David Buss, of Texas University, USA, in the first serious study on the frequency with which people try to attract an already-paired person as a partner, revealed that such behaviour is very common. They found that 60% of men and 53% of women admitted having tried on some occasion to lure away someones partner with a view to having a long-term relationship with them. However, when people were asked about doing so with only short-term sexual relations in mind, the percentage of men who admitted doing so remained high (60%), but the percentage of women so engaged was much lower (38%) (Schmitt & Buss 2001). Jealousy is a much more frequent and well-studied phenomenon, and infamous for giving rise to a great deal of violence. Many men have perished across history in fights (or duels) driven by jealousy. Many women have also died for the same reason at their own husbands hands and some men too have also been killed by their wives. For example, in Canada, of 812 women murdered by their husbands between 1974 and 1983, 195 (24%) died because of the husbands sexual jealousy. Of 248 men killed by their wives during the same period, jealousy was the motive on 7.7% of occasions (Daly & Wilson 1988). Jealousy has been interpreted by some evolutionary biologists as an adaptation that reduces the chances of extra-pair copulation. A jealous woman or a jealous man may be expected to keep a close eye on a partner. As evolutionary theory predicts, the motives that give rise to jealousy differ between men and women. Bearing in mind that certainty of maternity is always absolute, whereas certainty of paternity is very far from being so, suspicion of infidelity may be predicted to be the chief provoker of jealousy in men, but not in women. For women the most important matter is ensuring that a pairs resources are supplied entirely for herself and for her children, as happens with females in most other species in which males also invest in parental care (see Chapter 6). It may thus be predicted that what concerns a woman most will be the suspicion that her husband may have become involved in a longterm extramarital relationship that will oblige him to divert resources to another woman. In accordance with these predictions, David Buss and his co-workers asked interviewees to imagine that their partners were cheating 57 them and were having sexual relations and emotional involvement with another person. When asked which of these two aspects of the relationship most concerned them, 60% of men and 13% of women responded that it was the sexual relations, whereas emotional relations were much more worrying to the women (87%) than to the men (39%) (Buss et al. 1999). These results have emerged from a large number of studies carried out in different countries, sometimes with different methodologies. For example, in one experiment persons were seated in a comfortable chair and were connected to sensors measuring such parameters as heart rate and skin conductance. They were asked to imagine various scenarios related to jealousy. These sensors, and others indicating anxiety and stress, recorded maximum levels in women when emotional infidelity was raised. The sensors recorded maximum levels in men when different sexual positions employed by their wives and lovers were mentioned (Pietrzak et al. 2002). 5.7.4.2. Cultural `adaptations Human societies, nearly all of which are dominated by men, have promulgated a great variety of regulations and laws and have developed many taboos all with the ultimate aim of guarding women against extra-pair sex. The chastity belt, a massive iron device employed in the Middle Ages, is perhaps the method that we most associate with mate guarding. On reflection, the belt is but a crude imitation of the plugs employed by males of many species, to which we referred above. Other more subtle `customs related to sperm competition strategies are the veils, burkas and other body and facial coverings of women, whose purpose is to render them less attractive to men. It is instructive that such coverings are only obligatory for women of reproductive age. Furthermore, in countries where such customs apply, women normally seldom leave the house and are always accompanied when they do so. Another `tradition favoured by female guarding, although a much more drastic one, is female circumcision or clitorectomy. This inhuman practice (so cruel that it is confined to our own species) succeeds in diminishing or nearly eliminating a womans sexual desire (something that male houseflies achieve in a much more subtle way). Another very exaggerated type of genital mutilation is infibulation, which consists of sewing up both sets of vulval labia, leaving an orifice only large enough to permit the passage of urine and menstrual flow. In this way, which is truly worthy of the script of a horror film, a woman is guaranteed to be a virgin when she marries. Undoubtedly, the preoccupation with guarding women is most evident in the mass of laws established by nearly all cultures to punish adultery, these treating it as an offence against a mans most valued property: his woman. Hence, adultery has often been punished by death. For example, according to Marco Schwartz, the Bible is full of stories of adultery and of edicts that forbid it. It is the seventh commandment of the ten given in the book of Deuteronomy, the punishment for both parties being death, in ancient times by burning, but later by stoning (Schwartz 2008). It is striking that nearly all known legal codes, from the code of Hammurabi (18th century BC) to the most recent, include articles condemning adultery and all consider the woman to be her husbands property, making him the victim of the crime. In most modern societies, there are grounds for divorce if a woman is caught in adultery but if her spouse is the offender this is not necessarily the case. Of course, any case of adultery involves one woman and one man, but always along human history, women have been punished much more than men. 5.8. Sexual selection by cryptic female choice As we have noted, the process of sexual selection that we studied in Chapter 4 continues after copulation within the female reproductive tract. Competition between males continues as sperm competition and selection by females continues in the form of sperm selection. The latter comprises not permitting just any sperm to fertilize an egg, but instead selecting the sperm most likely to generate superior development of the offspring. This process is known as sexual selection by cryptic female choice, cryptic since it is not readily detectable. The ingenious idea that females, after copulating with several males, may be able to select the sperm with the best genes to fertilise their eggs was popularised by William Eberhard, of Costa Rica University. In his book, Eberhard (1996) highlights that insemination is no guarantee that eggs will be fertilised and he describes some 20 mechanisms by which females may control processes associated with fertilisation. Some, such as deciding when copulation ends or expelling the sperm of some males, are directly observable. Others, however, are invisible. These include whether or not sperm of a particular male is transported to sperm storage structures, selecting sperm and favouring or blocking the development of a fertilised egg. These remain speculative possibilities without direct supporting evidence, since sperm that succeed in fertilising the available ova may be those that succeeded in competition between spermatozoa, or that were selected criptically by the female, or both of these at once, so it is very difficult to know. At any rate, there are some findings supporting the idea that a female may select between sperm in some way, even if the mechanism is unknown. For example, Mats Olsson, of Gothenburg University, Sweden, and his co-workers studied genetic similarity, an indicator of relatedness, and paternity in the sand lizard (Lacerta agilis). This species is highly promiscuous and females will even mate with close relatives. The researchers found that the more closely related males fathered a smaller proportion of the offspring than did more distantly related males (Olsson et al. 1996). These results show that selection of sperm was occurring within the female reproductive tract. Another study, this time experimental, has shown the existence of cryptic selection in the small red damselfly (Ceriagrion tenellum), a member of the order odonata. In this insect group, males have been regarded as dominating fertilisation on account of their complex reproductive apparatus, which includes a diversity of structures adapted to withdrawing the sperm of other males that have copulated previously. Some examples of these adaptations were discussed earlier. Considerable variation is known to exist in the duration of copulation in this damselfly, which may last from 30 minutes to three hours. José Andrés and Adolfo Cordero Rivera, of Vigo University, Spain, carried out a series of 58 experiments under laboratory conditions to test four hypotheses that might account for this high variability. The two hypotheses that are most related to the subject of this chapter were, firstly, that the longer a male copulates the more effective he is at withdrawing the sperm of rival males that preceded him, and, secondly, that lengthy copulation favours preferential selection of the sperm by the female, i.e. cryptic selection. Both hypotheses predicted that the longer the duration of copulation, the more eggs would be fertilised, which was indeed the case. However, laboratory tests established that males only need ten minutes to withdraw rival sperm from the spermathecae, the females sperm storage organs. Thus sperm withdrawal could not explain the lengthy duration of copulation. The conclusion reached was that prolonged copulation fertilises more eggs because cryptic selection by females favours the ejaculates of those males that have spent longest in the act (Andrés & Cordero Rivera 2000). Only one study so far has shown one of the mechanisms of cryptic selection that takes place within the female reproductive apparatus. Danièle Carré and her collaborators at Pierre et Marie Curie University of Paris, France, studied a comb jelly (Beroe ovata), a marine animal of the phylum Ctenophora, whose eggs are transparent and large (1mm in diameter), allowing the process of fertilisation to be observed directly in the laboratory. It was found that once several sperm have attached to the ovum a series of changes occur in the ovum membrane near each sperm leading to, among other things, gatherings of mitochondria around the pronucleus of each sperm. The pronucleus of the ovum next moves quickly straight the egg cytoplasm to visit one or more of the attached male pronuclei. Sometimes the ovums pronucleus returns to a sperm pronucleus that it has already visited in order to fuse with it. This seems to be a clear demonstration of an ovum selecting which spermatozoan will fertilise it (Carré et al. 1991). Although scant proof exists of the importance of cryptic sperm selection by females, this is not to say that this is an unlikely evolutionary phenomenon or that generalisations cannot be made. The lack of proof is the inevitable consequence of the lack of suitable techniques for investigating a process that occurs concealed within the female genital tract. In addition to what evidence we have described, other data support the idea that selection by cryptic female choice is an evolutionary phenomenon of great relevance, as is sperm competition. Firstly, the female genital apparatus shows great morphological variation and complexity in most species, especially regarding the route that sperm must travel. The female reproductive tract usually consists of a tube presenting numerous obstacles, which zoologists and doctors have considered to be a surprisingly hostile environment for the sperm. A logical explanation is that the female reproductive tract amounts to a selective medium that eliminates the less competent sperm. A second argument in favour of cryptic selection is that although many sperm, which may derive from different males, reach the ovum, only one of them actually fertilises it. Females would gain an advantage by being able to select the sperm that bear the best (or most compatible) genes to fertilise the egg since this would increase the chances that the fertilized egg would develop into an offspring of higher quality, which might itself survive to be a breeding adult. 5.9. Fertilisation without courtship: alternative strategies Before closing this chapter we shall consider a topic of great interest to behavioural ecologists, that of alternative strategies. The term refers to the fact that not all individuals of a given species behave in the same way. Each may employ different ways to solve the same problem. We could have studied this topic in other chapters since it also applies to other aspects of behaviour. However, I have decided to deal with it here since competition to fertilise eggs offers particularly abundant and peculiar examples of alternative mating behaviours. We have seen that, as a general rule, before a male can fertilise a female he has to succeed in being selected by her and, after copulating, he must ensure that it is his sperm that fertilises her eggs. Both these stages imply competition, the former between males and the second between ejaculates. As we humans well know, to win a competition it is very important to have some sort of advantage over ones rivals. Animals do not base their behaviours on premeditated decisions but rather on evolutionary strategies, which are transmitted from generation to generation when they are effective and provide benefits to the individuals that employ them. The following example will help us to understand the topic better. In many animal species in which the males attract females by means of sounds, as happens with frogs and other tail-less amphibians, there often exist individuals, known as `satellite males, that do not call. These silent satellites take up positions close to singing males in order to intercept females that the latter attract. This behaviour seems sensible when we consider what the song signifies and that not all individual males are equally dominating or attractive. When a male toad or frog sings during the courting season he is sending the following message to both males and females of his species: `Hear my song; it shows that I am a large, strong male. The song nonetheless has different significance to either sex. To females he is saying `come and mate with me, but to males he means `this site is occupied and if you come near you will have to fight me. Imagine now a small weak male who is also keen to reproduce. Would it be wise for him to take up a position and sing? In this case, as pointed out in Chapter 4, the song is an honest signal of his physical condition and all he would be doing is indicating his low quality. His song would serve to advise females not to approach him and would inform males that his site is occupied by an easily displaced rival. Clearly the best thing such a male can do is to keep quiet. This then is why satellite males keep silent, because when a male with a more attractive voice than theirs is near it pays the satellites to keep quiet and to try to intercept females that pass by headed for the singing male. These sorts of strategies are very widespread in the animal kingdom, raising the key question `how can alternative strategies exist?. It might be supposed that the less effective alternatives would be eliminated by natural selection. There are three possible answers to this question and we shall consider each in turn. 1. Often, juvenile individuals, whose development is not yet complete, are not ready to compete with the larger and more experienced adults. It is thus adaptive that they should avoid direct confrontations and instead 59 employ alternative tactics. This may apply in the case of the satellite male frogs described above, as they could be young individuals that will engage in direct competition by song when they have grown. Another example involving individuals that have not yet developed fully has given rise to a fascinating behavioural adaptation in the marine iguana (Amblyrhynchus cristatus). Martin Wikelski and Silke Bäurle studied their mating system and found that males gather in groups in which each iguana defends a small territory. Females visit the group in order to mate with one of the males (an example of a lek mating system ­ see Chapter 6). Copulation takes about three minutes and competition between males is very strong, so that when one is mating those nearby attempts to displace him. Dominant males perform most of the copulations since the females prefer them and they are able to complete copulation successfully on 95% of all occasions, despite disturbance by other males. Smaller males initiate fewer copulations, but in addition, other males succeed in displacing them 29% of the times, before they have had time to ejaculate. In these circumstances, young male iguanas have developed a satellite behaviour, they wait around the boundaries of the territories of the dominant males and try to intercept approaching females. None of this is particularly unusual and similar satellite behaviour is common in many species. What is surprising is that, when a female appears, these satellite male iguanas masturbate to ejaculation before she approaches. They retain the viscous mass of semen at the entrance to the cloaca so that if they succeed in mounting a female they can transfer their sperm immediately, in much less than the three minutes that it normally takes. This tactic allows them a chance to fertilise the female before the dominant males intervene to separate them. This behavioural option increased the reproductive success of the satellite males by up to 41% (Wikelski & Bäurle 1996). 2. Two or more evolutionary strategies may coexist because each is effective depending on local environmental conditions. The American cricket story described in Chapter 10 is a good example. Something similar applies in the case described above of amphibians in which some males are vocal but other, satellite males, keep silent. Here the short-term reproductive success of vocal males is greatly superior to that of the silent ones but the former also run a high risk of being parasitized by a fly that kills them (see Chapter 10). Which of these two strategies will be favoured by natural selection? It depends. If flies are scarce, the vocal males mate the most. However, if there are many flies, the best tactic is that of the silent males because as they may attract fewer females they do not attract the killer flies. 3. Two or more strategies may coexist if they are in an evolutionary equilibrium, and this is the commonest explanation for the alternative tactics that we observe in nature. For example, there are many fish species in which the males defend a small territory, build a nest and care for the eggs and later for the young. Males of such species court females to induce them to lay their eggs in the nests that the males built. At that instant the male fertilises the eggs and from then on he dedicates himself to his charges. As it happens, however, an alternative strategy has been described in over 100 fish species that have this reproductive arrangement; the alternative is employed by smaller males known as `sneaks. The sneaks do not compete for territories but instead hide near territory holders. When they see a territorial male courting a female they wait until the moment when she lays her eggs. They then rush out of hiding and release their sperm over the eggs at the same time as the nest owner. The issue is complicated further by a second alternative strategy in some species. For example, in the bluegill (Lepomis macrochirus), a freshwater fish, in addition to sneaks there are also males that have the size and morphology of females (employing the `transvestite male strategy. See Chapter 10 for a detailed treatment). Given that males using different strategies all release sperm at the same time, sperm competition must be intense and natural selection will have favoured those individuals capable of producing a larger quantity of sperm. The enormous sexual dimorphism that exists between territorial males and sneaky males in the marine toadfish (Porichthys notatus) is surely the result of such sperm competition. According to a study by R. Brantley and A. Bass of Cornell University, USA, territorial males are eight times larger than the sneaks but the sneaks have enormous testes, seven times bigger than those of the territory holders (Brantley & Bass 1994). Indeed, the sneaks could be called swimming testes. A different tactic, the `pirate male, has been described in other species. Pirates are larger than territorial males and their strategy consists of attacking males when these are guarding their nests, fertilising the eggs and then leaving so as to return the nest to the care of its proprietor (van den Berghe 1988). Two or more of these strategies (sneaks, transvestites and pirates) can coexist in a population if they are in an evolutionary equilibrium, in which case the reproductive success of each kind of male will be about the same. This outcome results from `frequencydependent selection, which favours the strategy that has relatively fewer practitioners. For example, in a population in which territorial males and sneaky males coexist, both strategies will have similar reproductive success if they are in evolutionary equilibrium. This equilibrium persists because if for some reason the proportion of territorial males increases, the sneaks will have more chances to fertilise eggs and so will leave more (sneaky) descendants, which restores the proportions to equilibrium. If, in contrast, the proportion of sneaks increases, there will be more competition between them and territorial males will become more vigilant, leading to the sneaks leaving fewer descendants and returning their numbers to a proportion that allows an approximately equal reproductive success to both strategies. This then is frequency-dependent selection, which is responsible for maintaining evolutionary equilibrium. 60 Chapter 6 Parental care and mating systems 6.1 Introduction We have previously studied problems associated with mate seeking (Chapter 4) and fertilisation (Chapter 5). This third chapter on the theme of reproduction examines the strategies associated with parental care and goes on to consider different mating systems, which differ according to the number and sex of individuals that make up a reproductive unit. These two topics are closely related but we shall study parental care first since it is then easier to understand the evolution of mating systems. Robert Trivers (1972) pointed out the inverse relationship between effort devoted to mating and that devoted to parental care. His `parental investment theory rests on some of the arguments that we considered in Chapter 4, for example that males have much higher reproductive potential than females and tend to invest less than their mates do on parental care. The theory is also based on the idea that while a female (or pair) is caring for a group of offspring, further offspring cannot be produced. In terms of evolution, reproduction is one of the most important activities of any living being. However, the time and resources available for this task are limited and must be employed effectively. The sum of the time and resources that an individual dedicates to reproduction is its `reproductive effort. This, in accordance with parental investment theory, has two components, `mating effort (an individuals lifelong investment in seeking mates), and `parental effort (its investment in caring for its descendants). Reproductive effort is thus the sum of mating effort and parental effort. Hence, if an individual devotes a great deal of time to parental care, it will spend little time on mateseeking, and vice-versa. In this respect the sexes differ because females devote most of their reproductive effort to parental care and males mainly invest in mating. Here lies the key to the link between parental care and mating system. Both sexes in monogamous species invest highly in parental care and little in mating. However, in polygynous species, in which a male mates with several females, the typical male invests very little in parental care and devotes practically all his reproductive effort to mating with as many females as possible. 6.2 Parental care Parental care comprises behaviour that parents undertake, at some cost to themselves, which contributes to increasing the survival chances and reproduction of their offspring. Parental care is very lengthy and costly in our own species, as in most mammals, but this is not the general rule. Most species are concerned only with laying as many eggs as possible and these are then abandoned to their fate. Parental care is characteristic of mammals and birds, but it is also observed in a diversity of other groups. These do not just include fish, amphibians, reptiles and insects, but also, much more rarely, some molluscs, polychaete worms, echinoderms and even sponges. Parental care is highly varied both in the degree of development that it attains in different groups and in the range of care provided. The main types and the animal groups in which they occur are summarised in Box 6.1. The great diversity of types of parental care in groups often thought to be non-parental is striking. Box 6.1 is only a general summary and does not go into details but some of the ways in which parental care has evolved deserve particular attention. For example, the classic scenarios of a bird carrying food to its chicks in its beak, or of a carnivorous mammal carrying prey home in its mouth, have only rare equivalents among other animal groups. Much more unusual adaptations have developed in some cases. For example, parental care is common among frogs of the genus Dendrobates and after the females have laid their eggs in the grass the adults care for the young and carry them to pools of water. In one species, the strawberry poison frog (D. pumilio), the female feeds the tadpoles when they hatch, but what is unusual is that she uses unfertilised eggs to do so. In other words, she produces special eggs that have no reproductive purpose and uses them to nourish her young (Weygoldt 1980). Another example of feeding the young goes a good deal further. The female of the spider Stegodyphus lineatus opens the egg capsule thirty days after the eggs have been laid and helps her young to emerge. These are not yet completely developed and depend entirely on her care. She feeds them for two weeks by regurgitating a liquid feed. Thereafter she allows them to feed off her own body and, before long, the young have devoured their mother entirely, leaving only her empty husk (Schneider 1995). Development of the young within the mothers body, as is typical of mammals, is a highly complex type of parental care that keeps the young secure from all types of external dangers during their development, which is when they are most vulnerable. The mammalian arrangement is not unique and many variations of this adaptation have been described (see Box 6.1). For example, there are several frog species in which development occurs within skin folds or within the males mouth, but there is a still more unusual case. In the southern gastric-brooding frog Rheobatrachus silus, the female swallows fertilised eggs or recently hatched tadpoles, whose development occurs entirely within her stomach. She eats nothing throughout this period and the stomach stops producing gastric secretions, until the well-developed young emerge through her mouth after several days (Tyler & Carter 1981). Even more extreme parental adaptations exist. In the mite Acarophenax mahunkai, a parasitoid of the eggs of a certain beetle, the young females remain inside the mother. The mites life cycle is quite complex, as is often the case with parasites. Steinkraus & Cross (1993) found that a female mite that get to introduce into a beetle egg starts to eat it and grows fatter. Within her 61 body some 30 of her own eggs develop, most of them giving rise to females (27.2 females and 1.7 males on average). Once the eggs hatch inside the mother, the females are fertilised by their brothers. The whole process takes four days during which the mothers body swells to twenty times its original size. She then bursts, releasing the young. The male young then die, but the females set off to find a female beetle laden with eggs, in order to repeat the process. Main category Provision of chemical energy, nutrients and/or food Specific types Occurrence Direct provision of food (prey) and/or water External provision of epidermal or other glandular secretions. Delivered via the mouth or anus. Internal delivery of secretions of the ovary, reproductive apparatus or special cells A placenta or similar system connected to the maternal circulation Nutrients delivered directly by the maternal circulation Supply of maternal or sibling tissue Directly from the parental body (nearly always by the mother) By means of nests that the parents build of decomposing vegetation Keeping offspring in hidden places or constructing or making use of refuges (nests, holes and burrows). Carrying offspring externally on the parents bodies Some arthropods and fish. Many birds and mammals. Some arthropods, fish and birds. All mammals. Some sponges. Some arthropods, fish, amphibians and reptiles. Some arthropods, fish, amphibians and reptiles. Most mammals. Some insects Supply of warmth that favours the growth and survival of offspring Protection of offspring from predators and inclement weather. Some molluscs, arthropods, fish and amphibians. Some reptiles. Many birds and mammals. Some crocodiles and a few birds. Some polychaete annelids, octopuses and arthropods. Many vertebrates. Some rotifers, arthropods, echinoderms, fish, amphibians, birds and mammals. Many invertebrates and vertebrates. eggs, and care continues after the fry hatch in many species. In the well-known case of seahorses (and their close relatives) females lay their eggs in the males abdominal brood pouch, where they hatch and the young develop. There are other less familiar examples that are no less fascinating. I was surprised by a television documentary that I saw some time ago. It showed the process of laying and egg fertilisation in a small, freshwater fish. The male and female leapt out of the water almost in unison, the female then laying her eggs on a leaf of some overhanging plant and the male brushing them with his sperm to fertilise them. These leaps went on for quite some time, given that the female could lay up to 300 eggs. I noted the species name, the splash tetra (Copeina arnoldi), and sought further information. I discovered that apart from this being very rare behaviour among fish (which the documentary was highlighting), males also perform unusual parental care in this species. After laying they remain near the eggs for three days and keeps on leaping, to brush them with water and prevent them from drying out (Krekorian 1976). By way of a final example of parental care performed by males we have the case of a frugivorous bat, the dyak fruit-bat (Dyacopterus spadiceus). This is perhaps the most unusual of all, at least from our point of view as mammals, since here the males help to suckle the young by producing milk of similar quality to that of the females. This seems to result from their eating plants that contain chemicals that stimulate milk production (Francis et al. 1994), but this proximate explanation leaves unanswered why males in this species have evolved the ability to be stimulated to produce milk. 6.2.1. Evolution of parental care We have seen that parental care presumably increases the chances that offspring will survive to breed successfully. The key question, therefore, is `why has parental care evolved in some species and not in others?. We can only give a very general answer: not all species are subject to the same selective pressures. We cannot really be more precise but evolutionary theory allows us to say that in species where parental care has evolved, the benefits obtained by the parents and the offspring must be greater than the costs incurred by the parents. That said, it is the case that the amount of parental investment is very variable among species in which it occurs and is also dependent on the relationship between the costs borne by parents and the benefits obtained by offspring. The selective pressures favouring the evolution of parental care are also very variable. The most important are surely associated with life in a hostile environment in which the living conditions are very difficult. The outcome of such influences as adverse climate and the presence of numerous predators and/or parasites, for example. There are also other pressures associated with the biology and evolutionary history of species, which may act at the same time as the environmental ones. In any event, the chief compromise is between the number of descendants produced and the degree of parental care. If the environment is favourable for the independent development of the young, parental care declines. Carrying offspring within the reproductive system, the gut, the ovaries, within special sacs or within other spaces inside the parents bodies Guarding and defending offspring Retrieving lost young Care of nest or offspring Provision of information important to survival or reproduction Fanning or irrigating offspring to aid thermoregulation, respiration, removal of excreta and to reduce infection risk. Nest cleaning and/or grooming the young to reduce risks of parasitism or disease By imitation of the parents or direct instruction by them. Some octopuses, arthropods and echinoderms. Many vertebrates. Some arthropods, fish and reptiles. Many birds and mammals. Some leeches, insects, octopuses and fish Some arthropods. Many birds and mammals. Many birds and mammals Box 6.1. The chief types of parental care and the animal groups in which they occur. After Glazier (2002). Nearly all of these examples relate to parental care by females. However, it is not always so and males in some groups often perform the task. Among fish, for example, it is common for males to guard, defend and irrigate the 62 6.2.2. Parental care by males: the importance of certainty of paternity Before addressing the conflict that exists between males and females with respect to parental care, it is worth highlighting a very important matter when it comes to the evolution of male parental care: their certainty of paternity (see Chapter 5). Given that parental duties are costly to males, the behaviour will only evolve if care is actually directed at their own offspring (i.e., their own genes). It may therefore be predicted that the level of parental care offered by a male will be related to his certainty of paternity. This idea has been tested both in comparative studies and by means of experimental investigations with many species in which the males confidence in paternity has been manipulated. In one of these latter studies, Bryan Neff, of West Ontario University, Canada, carried out a brilliant study of a freshwater fish, the bluegill (Lepomis macrochirus), whose males care for and defend the eggs and young. In this species, in addition to males that court females, there are `sneaky males (those that fertilise eggs laid by a female who is being courted by another male; see Chapter 5), so that absolute certainty of paternity is impossible. In one of Neffs experiments, the presence of a sneaky male near to an experimental nest was simulated. In the another experiment, a third of the eggs were exchanged with those from other nests, bearing in mind that male bluegills can distinguish eggs by smell. Both experiments also employed unmanipulated nests as control groups. In order to quantify parental care, a live predator was presented within a transparent bag and the nest owners behaviour was observed in order to produce an index of their investment in defence. As predicted, both types of manipulation significantly affected the intensity of the parental care performed. Males were less defensive when they had observed a rival male near the nest when the eggs were laid and also when they had detected strange eggs in the nest. 6.2.3. Which sex provides parental care? The conflict between males and females By definition, parental care can help offspring survive to reproduce, and thus contributes to the genetic success of both parents, the male as much as the female. However, such success arises independently of who provides the care. Natural selection does not favour the most successful pair, but rather the individual who leaves most descendants. It is therefore unsurprising that there is significant conflict between males and females, given that selection will favour the individual who is capable of getting its mate to invest more in parental care than it does itself. That individual can then invest more in seeking more mates and thus will leave more descendants. A review of different animal groups reveals enormous variation regarding which sex cares for the young. For example, it is usually provided by the male in those fish in which there is parental care. In birds usually both sexes participate, whereas in mammals it is nearly always just the female who cares. This variation is the outcome of the evolutionary conflict between males and females in which each sex tries to ensure that it is the other that provides parental care. Why have males won this conflict in most species? Perhaps because biological, physiological and other factors predispose females to be the carers (see Box 6.2). Why is parental care in birds provided by both sexes but solely by males in fish? Several factors may be involved and these give rise to various hypotheses. Where birds are concerned there is a particular hypothesis that applies quite generally although not to all species. The situation in fish is less clear (See Box 6.3). In general, we can say that parental care is provided by only one sex when it is not essential that both should participate. In this circumstance, when one sex has the opportunity of finding another mate and of deserting, it will leave the other sex to care for the offspring. 1. Biological and physiological factors predisposing females to be carers a. Males have the possibility of deserting earlier in species with internal fertilisation. b. Where gestation is internal, as in mammals, females are predisposed to provide parental care since the young develop within them. This makes it easier for the male to abandon one partner to seek other mates. 2. Other factors c. Males are much less certain of their paternity than females are of their maternity. d. Males have more opportunities than females to pair again and they have more to gain from doing so. e. The costs and benefits of parental care are not equal for males and females. The costs are typically higher for males and the benefits higher for females. Box 6.2. Factors that favour the evolution of exclusive female parental care in most species. Matteo Griggio, of the Konrad Lorenz Institute of Ethology, Austria, and Andrea Pilastro, of Padova University, Italy, have published several studies of parental care in the rock sparrow (Petronia petronia). Both sexes in this species apparently have opportunities to desert their partners because some nests are attended by the male only, others by the female only, and still others by both sexes jointly. This species thus provides an interesting model for trying to understand how the division of parental care between both sexes evolves. Why is parental care in birds provided by both sexes? - Influencing factors: Parental care in birds is highly elaborate and costly. It involves building a nest, incubating the eggs for 24 hours a day and then feeding the chicks, which grow very rapidly and thus have voracious appetites. - Conclusion: The most widely accepted hypothesis is that biparental care has evolved in birds because the investment required by the offspring is so large that both parents are needed to provide it. Why is parental care in fish provided by the male? - Influencing factors: o Fertilisation is external, not internal, so the female has the first opportunity to desert, leaving the male holding the eggs. o The female lays her eggs in a nest built by the male in his territory. The male continues to defend the territory and the nest while trying to attract more females so performing parental duties that only consist of defending and oxygenating the eggs is less costly for the male than for the female. - Conclusion: Three explanatory hypotheses have been suggested. The carers are the males because (i) they have a high certainty of paternity, (ii) they release their gametes after the females do, and (iii) they are physically more closely related to the embryos. The third hypothesis has attracted most support. Box 6.3. Influencing factors and hypotheses explaining the distribution of parental care in birds and fish. After Krebs & Davies (1993). 63 In the rock sparrow, as with most species, males desert more often than females. The investigators identified the principal reasons why. The females incubate the eggs and brood the chicks during their earliest days, so the males are the first to have an opportunity to desert (Griggio & Pilastro 2007). When either sex deserts, a new breeding attempt with another partner begins. Thus the benefits of desertion are limited by the availability of individuals of the opposite sex with which to pair. The investigators found that females desert more often when there are more available males (Pilastro et al. 2001). Finally, they found that desertion is costlier for females than for males since, when a male deserts the female compensates for his absence by increasing the number of feeds brought to the young, so favouring the survival of the entire brood. However, when a female deserts the male only partly compensates for her absence and therefore some of the chicks are likely to die (Griggio & Pilastro 2007). 6.2.4 Parent-offspring conflict and sibling conflict The `parent­offspring conflict theory that Robert Trivers (1974) proposed, maintains that although survival is what matters to offspring and that offspring survival is vital to their parents, the interests of both parties do not completely coincide. Trivers argued that the optimal strategy for parents is to invest equally in all their offspring, including those that have yet to be born, since all of them share 50% of the parental genes. On the other hand, the optimal strategy for each of the offspring is to receive more parental investment than their siblings, given that an individual is obviously 100% related to itself, but shares only 50% of its genes with its brothers and sisters. This implies that natural selection can favours offspring that demand and receive greater parental investment from their parents than the latter are disposed to provide. It also implies that selection will have favoured those parents that have developed counter-adaptations to avoid blackmail by selfish offspring, given that parents who give in to individual offspring at the expense of the others will leave fewer descendants than those that distribute resources equally. In other words, offspring have evolved to demand more from their parents than these have been selected to provide; and parents have developed counter-adaptations to resist such demands so as not to endanger the survival of the remainder of their young as well as not harming their own reproductive future. One of the best-studied aspects of this conflict concerns the duration of the period of parental care. Offspring prefer to prolong this period as much as possible, but it is in the interests of parents to cut short their investment in offspring as soon as these are capable of fending adequately themselves, with a view to beginning investment in further offspring. This strategy allows parents to increase the number of breeding attempts that they can make throughout their lives, thus leaving more descendants. A typical example of the conflict associated with the duration of parental care arises from the timing of weaning in mammals. Most of you who have bred dogs or cats will have noted that once the puppies or kittens have grown, they nevertheless keep trying to suckle, while their mother makes it harder for them and allows them to do so for progressively less time, until at last she stops altogether (although if only one offspring has been left with its mother the latter is much more indulgent). This independence conflict of offspring is not confined to mammals, but is widespread throughout the animal kingdom. Another good example comes from a study of a predatory bird, Montagus harrier (Circus pygargus) by Beatriz Arroyo (then of the Centre for Ecology and Hydrology at Banchory, UK), and her coworkers. In this species, as with other birds in which the chicks develop within a nest, the young are attended by their parents for a more or less prolonged period after they have fledged, until they become independent. The investigators found that the young attempted to prolong the period of dependence on their parents, especially when the food supply was scarce. As time went on the young improved their flying and hunting ability, but kept on soliciting food from their parents. Nevertheless, the parents eventually reduced the frequency of feeds, provoking more aggressive demands for food from the young, even though their parents had stopped feeding them some days later (Arroyo et al. 2002). Given that for each offspring the optimum situation is to receive more resources than its siblings, parent­offspring conflict predicts that the latter will have to compete among themselves in order to secure a larger share of what the parents provide. This conflict is seen very clearly in birds, especially in those in which hatching is asynchronous because the female begins incubation before the clutch is complete. In such species some chicks hatch earlier than others and, being larger, have an advantage when competing for food. Such competition often leads to the death of one or more of the smallest chicks. Sibling conflict is most severe in some species with asynchronous hatching where the older sibling itself often kills the younger one. Sibling conflict has been studied in other animal groups, particularly in mammals. Fritz Trillmich and Jochen Wolf, respectively of Bielefeld and Cologne Universities, Germany, carried out an exemplary study of this conflict in two marine mammal species, the Galapagos fur seal (Arctocephalus galapagoensis) and the Galapagos sea lion (Zalophus wollebaeki). The females of both species do not wean their young until these are two years old, by which time they themselves may have given birth again. In about 23% of cases a female finds herself caring for a two-year-old as well as for a newborn offspring. In such cases sibling conflict reveals itself in various ways. For example, the younger sibling weighs less at birth and grows more slowly than those whose mothers are not also feeding a larger brother or sister. Younger pups with siblings also suffer higher mortality, either through competing unsuccessfully for food or as a result of being attacked by the larger sibling. This was especially so when food availability was lower and also when the larger sibling was a brother and not a sister (Trillmich & Wolf 2008). The same study also revealed the conflict between the mother and her offspring. As parent-offspring theory predicts, the mother served her own interests, by defending the smaller pup against aggression by the larger one and, if the latter was sufficiently developed, by ceasing to feed it and forcing it to become independent. On the other hand, if the larger pup was not yet capable of independence, the mother might abandon the smaller one, leaving it to die (Trillmich & Wolf 2008). 64 6.2.5 Human parental care All of you will acknowledge that we humans care for our own young, as do other animals. However, if I maintain that Trivers parental investment theory also applies to human parental care, I am sure that not all of you will agree. We shall return to this matter at the end of this section. Let us start by asking ourselves a question: `why do we care for our children? Most parents will immediately reply `because we love them. However, this does not resolve the matter from a scientific point of view since we need to consider the deeper significance of `we love them. Before answering the question I will put another that is fundamental to assessing the relationship between human behaviour and that of other animals: `Is it a conscious decision, made because we are inclined that way by our intellect and by our most sublime rationality, or is it in some way instinctive as in other animals? We shall examine the neurohormonal changes that result from the birth of a child, in order to answer these two questions. The principal changes are given in Box 6.4. If we look at these carefully we can see that many of the changes that take place in mothers prepare them for enjoying the experience while they perform the heavy onerous tasks that caring for their babies involve. To illustrate the latter I can supply a little-known fact: first-time mothers lose 700 hours of sleep on average during the babys first year. Moreover, bearing in mind the neuro-hormonal changes given in Box 6.4, it is not surprising that having and caring for a baby is so gratifying to mothers, since maternal love has much in common with romantic love (both activate the same parts of the brain). Andreas Bartels and Semir Zekiof, of University College London, UK, studied mothers who had recently given birth, using a modern scanner to record cerebral activity. They presented the mothers in turn with photographs of their own babies, of their romantic partners, and of other babies and of friends, in order to compare their responses. They found that both photos of own babies and of partners activated different parts of the brain but both of these, and not the control photos, activated the same reward zones that comprise areas rich in oxytocin receptors, this being the hormone that produces intense feelings of satisfaction (Bartels and Zeki 2004). Neurohormonal changes in fathers also increase their willingness to care for and defend the baby (see Box 6.4). It appears that in men such changes are brought about by pheromones produced by pregnant women. Box 6.4. provides the answers to our two earlier questions. We certainly care for our children because we love them but that `love is the outcome of an evolutionary process that has favoured both mothers and fathers with the proximate neurohormonal systems that encourage parents to take care of their offspring. For example, the babys cry provokes an immediate physiological response in its mother that alerts her to the need to attend to it. Such a response depends on a complex interaction between external stimuli, the nervous system and hormonal influences and may thus be very flexible. That response may also operate in the father if he is conditioned to the need and may not do so in the mother if she thus feels liberated from that need. A personal anecdote may illustrate this flexibility clearly. My second child was born thirteen months after the first. Since my wife had to return to work after her maternity leave we agreed that, at night, she would get up if the younger child cried and I would do so for the elder one. My wife had to wake me for the first few nights but, to our surprise, only two weeks later on most occasions each of us only woke up when `our baby cried and not when the `other one did so. Changes in mothers 1. Dopamine (the substance responsible for pleasure and reward) levels rise due to the effect of oestrogen and oxytocin (this is the same reward circuit activated during intimate communication and by female orgasm). 2. Oxytocin is released in great quantities during lactation (as it is during orgasm) and causes the sensations of love that all mothers feel towards their babies and triggers protection and care of the young. 3. Breast-feeding reinforces maternal behaviour. When the baby starts suckling, great quantities of oxytocin, dopamine and prolactin are released in the mother. The first two make her feel loved, link her physically to her child and make her emotionally satisfied, so that sexual desire declines. Many of the emotional benefits that sexual relations used to provide are now provided by motherhood. 4. Breast-feeding lowers blood pressure, tranquilises the mother, makes her feel relaxed and stimulates an intense feeling of love for the baby. Changes in fathers 1. Levels of prolactin (the child-raising and lactation hormone) increase by 20% during the weeks preceding the birth, stimulating strong sensations of love for the child even before it is born. 2. Levels of cortisol (a stress-related hormone) may double, stimulating sensitivity, alertness and concern for the babys security. 3. Testosterone levels fall by a third and oestrogen levels rise above normal during the first few weeks after the birth. (Testosterone increases sexual drive and represses maternal behaviour). This reduces the need to have sexual relations and increases concern and affection for the baby. Box 6.4. Neurohormonal changes that occur in the female and male brain towards the end of pregnancy and after birth. Chiefly after Brizendine (2006) and Goleman (2006). The hormonal basis and the flexibility of the parental behaviour that we have studied indicate that, as in all other animals, parental care in humans is the result of natural selection. It thus supports the initial assertion, that human parental care may also be analysed from the evolutionary approach of Trivers parental investment theory. 6.2.5.1. The evolution of human parental care We shall now consider various matters arising from Trivers theory that we studied earlier in other animals. In the first instance, we highlighted the importance of paternity certainty on the evolution of parental care. Evidence suggests that certainty of paternity influences decisions on parental care by we humans. A man invests less in parental care when he believes that his children are not his genetic offspring. For example, many studies have revealed that men invest less in their stepchildren than in their own children and that children living with an adoptive father are more likely to suffer maltreatment and to die than those who live with their biological father (see a detailed account in Chapter 1). These are cases in which certainty of paternity is absolute and thus the behaviour may derive from a conscious decision. However, as in other animals, positive or negative indicators of paternity have been found to be influential. A study by Coren Apicella and Frank Marlowe, Harvard University, USA, provides a good example. They investigated the influence on 65 parental care on two factors associated with probability of paternity. These were a mans perception of how much his children resemble him and also his perception of his wifes fidelity. A group of 144 men was presented with a questionnaire designed to evaluate each mans view of three aspects important to the study: his resemblance to his children, his wifes fidelity and his investment in parental care. Each man was presented with a series of statements to which a value of 1 to 5 had to be assigned, on a scale ranging from `totally agree to `totally disagree. An example of the statements, relating to the mans resemblance to his children, was: (a) `I think my children resemble me more than their mother, (b) `I think my children have some of my personality traits, and (c) `many people think my children resemble me. The predictions based on Trivers theory were also met in this study. Men invested more in parental care, by paying more attention to the children and spending more time with them, when these men thought that the children resembled them and that their investment was lower when they thought that there was not much resemblance. The second prediction was also fulfilled, men who were more confident of their wifes fidelity dedicated more time to their children than did those who were less certain (Apicella & Marlowe 2004). We have also previously studied the relationship that should exist between parental effort and effort to secure mates, according to the parental investment theory. This too has been demonstrated in humans, both in modern developed societies and in hunter-gatherer societies, where investment by men in parental duties is influenced by the availability of women as potential partners (as happens with the rock sparrow). Men who consider themselves to be very attractive invest less in caring for their children and instead invest more in seeking more partners, than do men who think themselves less attractive. A good example was provided by Frank Marlowe, one of the investigators in the previous study, who worked with the Hadza, a hunter-gatherer people in Tanzania. He found that adopted children received less care than biological children, a finding confirmed by many other studies. He also found that the more women of fertile age there were in a village, the less time fathers spent with their children (Marlowe 1999). This result shows that there exists conflict between paired men and women (fathers and mothers) regarding care for their children, and it supports Trivers general prediction that there should be a negative correlation between parental effort and mating effort. 6.2.5.2. Human parent-offspring conflict In humans, as in other animal species, both parents and offspring derive important evolutionary benefits from parental care. The offspring benefit since parental care improves their chances of survival to breeding age, whereas the parents benefit since they increase the chances of producing successful descendants. One might therefore expect both parties to facilitate parental care; the offspring should cooperate with their parents and should look after them in a way that would be optimal for both. Nevertheless, this cooperation does not happen in humans any more than it does in other animals. We shall consider what does occur in our own species since I believe that it is a most important topic and a highly topical one. As we all know, raising children properly is very difficult. If we over-protect them they may become spoilt, demanding and impossible to satisfy. At the opposite extreme, if we neglect them they may even die for lack of love and companionship as has occurred in orphanages set up for foundlings and other abandoned children. For example, there is very clear and reliable data that reveals that in the United States, during the early 20th century, nearly all children taken in by such orphanages died before they were two years old. Why is raising children so hard? The simple answer, without going into details, is because this activity is fraught with conflict. There is conflict between the father and the mother (as in the case of the Hadza above), conflict between siblings and, most important of all, between parents and offspring. Does the parent-offspring conflict that we have described for other animals also exist in humans? Some may not see this clearly but the answer is a resounding `Yes. It begins at the moment of conception and continues throughout life (see Box 6.5). By way of example, Box 6.5 presents some apparent examples of conflict between mother and foetus. This information, the fruit of modern medical investigations, should convince the most sceptical of the existence of such conflict. They reveal that the foetus has evolved mechanisms to secure the greatest possible supply of resources from its mother, who in turn has developed mechanisms to avoid excessive exploitation by the foetus. Mother-child conflict continues after birth. For example, babies attempt to obtain as much milk as possible from their mother. In the face of excessive demand she secretes benzodiazepine in her milk, a substance that has a sedative effect. Babies have been shaped by natural selection to obtain what they need. On the one hand, their cry is highly effective in gaining the attention of the mother and father. On the other, their smiles and cuddling give great pleasure to their parents, which help insure that the joys of parenthood exceed the disadvantages. In other words, babies possess suitable adaptations for making themselves loved, which are clearly worthwhile since only babies whose parents love and care for them are likely to reach adulthood. 6.2.5.2.1 A warning about the parent-offspring conflict There is a very worrying side to parent-offspring relations in modern western societies. To explain this we shall first consider what may have been the relationship between mothers and suckling babies during the Stone Age, based on what we know of the Bushmen and other modern hunter-gatherers. Mothers, with babies in arms, spent many hours searching for and collecting food. The babies often cried and would be immediately suckled when they did so, three or four times an hour for one or two minutes at a time. Mothers did not have large food reserves but rather depended on what they gathered daily. Moreover, mothers with babies very often also had an older child, some four years old, to care for. Life was very hard and there would have been periods of scarcity during which the children would have gone hungry and been otherwise in need. The adaptations that 66 babies possess to make themselves loved and to secure the greatest parental investment possible evolved in such circumstances. Mothers (and fathers) were also adapted to respond quickly to their babys begging cries since, in times of scarcity, descendants were only produced by those parents who were capable of meeting their childrens needs quickly and effectively. A. Conflict in the mother 1. Defective embryos are aborted (from 30% to 75% of embryos are aborted spontaneously). Genetic studies of foetuses that abort have shown that a high proportion have genetic defects. It is thus best for the mother to abort rather than to continue investing in an embryo with little chance of survival. 2. The greater the maternal blood flow to the placenta, the more nutrients available to the foetus. The mother tends to reduce her blood pressure, which prevents the foetus securing too great a share of resources and so prejudicing her health. 3. When a non-pregnant woman consumes a carbohydrate-rich meal her blood sugar level rises rapidly, and then falls on account of insulin, which stimulates the conversion of sugar to glycogen, which is stored in the liver. Pregnant women are less sensitive to insulin and have to increase its levels in their blood. 4. Some 70% of pregnant women suffer nausea and vomiting during the first three months of pregnancy. This happens precisely during the period when a foetus is most vulnerable and, especially, in response to substances most likely to be toxic to it (meat, eggs, strong-flavoured vegetables, coffee and alcohol). B. Conflict in the foetus 1. High maternal blood progesterone levels help to sustain the pregnancy. When the foetus is sufficiently developed it releases gonadotropin, a hormone that stimulates maternal progesterone production, and so contributes to this process. 2. From the moment of implantation, the foetus stimulates a dilation of the maternal arteries and an increase in maternal blood pressure, enabling it to secure a greater supply of resources. 3. The placenta produces a hormone that reduces the mothers sensitivity to insulin, thus ensuring a larger supply of glucose to the foetus. Box 6.5. Conflict between mother and foetus. The first three points in both sections are matching adaptations and counter-adaptations. Point 4 in section A may not be a case of conflict since it may not be instigated by the foetus, as it could be a response of the mother since it increases the chances of a successful pregnancy. After Cartwright (2000) and Barret et al. (2002). changed their begging strategies and continue to be very demanding. Parents tend to respond to all signals of need (cries) from their children but the latter have evolved to beg and demand, which means that they will continue to do so even after their basic needs have been met. They may be neither hungry nor ill or cold, the basic causes that made them cry in the Stone Age, but they have other needs that come to acquire more importance for them, such as being picked up, being fed certain favourite foods or getting more toys, and they cry to obtain these. Parents may give in to all these whims but the children do not necessarily stop crying but rather cry to demand less important `needs. The conclusion is that children will never stop crying however much some parents respond by satisfying all their childrens demands. Children have evolved to be effective at begging and they will continue crying and to be more demanding with each passing day. Parent-offspring conflict, with respect to the period during which children remain dependent on their parents, also arises as a consequence of modern living circumstances in our opulent western societies. Numerous studies have revealed that children become independent much later than used to be the case. For example, according to the Youth Institute (`Instituto de la Juventud) in Spain, now only 23% of young people have left home at the age of thirty. This dramatic statistic reveals an enormous change since only thirty or forty years ago children became independent to start their own families soon after they reached the age of twenty. The reasons are various, but perhaps the most important change is the same as we mentioned earlier: parents are disposed to invest more in their children. They give them every opportunity to stay and so it is much more convenient for them to do so instead of becoming independent, especially considering the difficulties mature offspring face in securing employment in todays economic environment. 6.2.5.3. Human sibling conflict As we have noted, Trivers parent-offspring conflict theory also predicts conflicts between siblings, given that each may try to secure more than its fair share of resources. Humans are no exception and conflict between human siblings is widespread. The history books record numerous instances of competition between siblings for rights of primogeniture, these even ending in murder. Psychologists are also well familiar with problems of jealousy between small siblings. Offspring also sometimes feud over the distribution of their inheritance. This is not to say, however, that the general rule is for human siblings to get on badly. On the contrary, they often collaborate and help each other for reasons that we shall discuss in Chapter 8. Quite a few studies reveal the existence of sibling conflict at various levels, although the topic has been less studied that parent-offspring conflict. We shall examine an example that meets one of the most drastic predictions of the theory, that having insufficient time between successive births increases the chances that one of the children will die. Noval Alam, of the Indian Centre for Population Studies, followed the lives of nearly 4,000 children who were born in a rural part of Bangladesh between 1983 and 1984. He found that if two children were born less than 15 months apart, the survival of the elder child increased the chance that the Things are very different in modern societies. Women go out to work and can neither take their baby with them nor can they keep stopping to suckle it. Other profound changes have also occurred. Abundant food resources are available. Women often wait until they are 30 years old before having their first child and the number of children born per woman has declined sharply (it is currently 1.3 per woman in Spain). We live under completely different conditions from those of our ancestors, in which parents need not be overly concerned with the survival of previous or future offspring, nor with their own. This change between primitive and current living conditions may explain differences between the parental care strategies of our ancestors and those seen in modern industrialised societies. Human parents nowadays are inclined to invest much more in their offspring than was the case in Prehistory, when limited resources had to be stretched to keep themselves alive and to feed several children. There will often have been times when there was insufficient food and breast-feeding mothers would have had trouble producing sufficient milk. The problem to which I drew attention in the section heading is that, although modern parents have changed their parental care strategies since they often no longer face limits to investing more, children have not 67 younger would die. However, if the elder died, the interval between births did not influence the survival of the younger. These findings were significant after controlling statistically for gender, the mothers age and familial economic status, so the conclusion was that the mortality was due to competition between the siblings for the available resources (Alam 1995). mating system for females is generally that in which males remain to deliver parental care, allowing the females to devote all their effort entirely to producing and laying more eggs, thus leaving a greater number of descendants (polyandry). The study that best highlights the role of intersexual conflict in determining mating systems is that by Nick Davies, of Cambridge University, UK, on the dunnock (Prunella modularis), a contemporary classic of behavioural ecology. This small bird does not have a fixed mating system. It is possible to find pairs, polygynous or polyandrous trios and polygynandrous groups (usually two males with two females), all within the same population. Nick Davies and his co-workers employed molecular analyses to establish the father and mother of each chick. They found that reproductive success was identical for both sexes in monogamous pairs (the male and female were each parents of an average of 5 offspring). In the polygynous trios each female was the mother of 3.8 chicks on average, whereas the male was the father of all of them, an average of 7.8 offspring. In polyandrous trios the reproductive success of the males depended on their dominance status (3.7 offspring for dominants and 3.0 for subordinates), and the female was the mother of all of them, an average of 6.7 offspring. Finally, in the polygynandrous groups the two females had the same reproductive success of 3.6 offspring each whereas that of the males once again depended on their dominance (5.0 for dominants and 2.2 for subordinates). Thus, as we noted earlier, a male achieved maximum reproductive success in polygyny whereas a female did so in polyandry. Bearing the above differences in mind, intersexual conflict is revealed to be the consequence of females trying to be polyandrous whereas males strive to be polygynous. Indeed, Nick Davies and his co-workers proved that once males have acquired their first female they are not content to remain monogamous, but continue to court other females in order to become polygynous males. Much the same occurs with females, who also are not satisfied with just one male and try to attract others to mate with them in order to become polyandrous. There is also significant conflict between same-sex individuals, given that it is better for a male to be monogamous than polyandrous and also better for a female to be monogamous than polygynous. Thus if a male attracts another female, the first female will try to drive her away. Similarly, if a female succeeds in attracting another male, the first male will attack him with a view to chasing him off. The resulting mating system depends on the aggression and degree of dominance of the females and males making up the group but it is also related to resource availability. A male with a food-rich territory has a good chance of attracting a second female and becoming polygynous. However, if the territory is poor there is more chance that the female will acquire a second male, who will also help to feed the chicks (Davies 1992). In general and as seen in the dunnock, polygyny is the outcome of a males victory in the inter-sexual conflict and polyandry represents the same for a female. Monogamy and polygynandry occur when neither sex proves capable of manipulating the other to its own advantage. What we have seen so far allows us to predict that in polygynous species the reproductive success of the 6.3 Mating systems Different mating systems are defined in terms of the number of individuals of each sex that comprise them. Box 6.6 gives the most usual classification, which is followed with minor variations by all textbooks. It is undoubtedly useful but it must be emphasised from the start that the limits between different systems are not at all clear-cut, and there may be considerable variation even within a particular species. This is unsurprising since mating systems may be seen as the evolutionary outcome of conflict between the sexes in specific ecological scenarios. The particular ecological conditions in each scenario will determine what sex wins the conflict in those circumstances. In other words, the evolution of mating systems is determined by ecological conditions because they directly affect the opportunities for males or females to manipulate the opposite sex or to escape manipulation by a partner. - Monogamy: One male and one female. Both sexes share parental care. May be annual (a new pair forms each breeding season) or permanent (pairing is lifelong). Relatively infrequent and only predominant in birds. - Polygamy: One member of one sex with several of the opposite sex. - Polygyny: One male and several females. Females deliver parental care. May be successive (one female follows another) or simultaneous (several females at a time). This is the optimal system for the reproductive success of the male. Occurs when males have the chance to monopolise several females. May involve pair formation but more usually the female is left alone after mating. - Polyandry: One female and several males. Males deliver parental care. May also be successive or simultaneous. This is the optimal system for the reproductive success of the female. Occurs when females are able to control access to themselves by males. This is the most uncommon mating system and occurs only in a few species of birds as well as a few species in other groups. - Polygynandry: Several females and several males. Both sexes share parental care but in mammals this is chiefly delivered by the females. A mixture of polygyny and polyandry. Also quite rare but less so in mammals, especially among primates. - Promiscuity: Males and females may mate with multiple partners without bestowing parental care on offspring. No parental care. Common in fish and in marine invertebrates. Box 6.6. Classification and definitions of animal mating systems. 6.3.1. Mating system conflict between males and females The key to understanding the evolution of mating systems is conflict between the sexes. We will thus begin by recalling some general aspects of that conflict (see Chapter 4 for a more detailed account). Males have higher reproductive potential than females so their optimal reproductive strategy is generally to fertilise as many females as possible and to leave them in charge of the offspring (polygyny). In contrast, females have a limited number of ova that require considerable investment, and they can only increase their reproductive success by getting males to care for the young, or at least to help with raising them. The ideal 68 most successful males will be greater than that of the most successful females, whereas the opposite applies to polyandrous species, where the success of the most successful females will be greater than that of the most successful males. Reproductive success will be similar in both sexes in monogamous and polygynandrous species. It is important to emphasise that reproductive success here refers to the success of individuals. At the population level, the number of descendants left by males is obviously exactly the same as that left by females. However, in polygynous species where a few males monopolise a larger number of females, the weaker males fail to reproduce. The same applies in the case of polyandrous females. Thus, polygyny and polyandry, the most successful systems for males and females respectively, are advantageous only for the stronger individuals since competition is fierce: the weaker leave few or no descendants. The lifetime reproductive success of males and females has been recorded for few species but what data exist support what we have just concluded. As evident in Box 6.7, in the kittiwake, a monogamous species, both sexes produce approximately equal numbers of young. The maximum number of young produced by a stag with a harem of hinds at his disposal is nearly twice that produced by each female (even though he is shorterlived). The maximum number of young produced by a male elephant seal, a highly polygynous species in which only a few males reproduce and these have large harems, is much greater than the output of any one female. The data on the human species refer to Moulay Ismael the bloodthirsty, emperor of Morocco, who had a harem of 500 women at his disposal and to Madalena Carnauba, a Brazilian woman, who gave birth to 24 sons and 8 daughters. The Guinness book of records cites a 19th century Russian peasant who is said to have had 69 children from 27 births (Krebs & Davies 1993), but the claim is regarded as unreliable by various experts. Common name Black-legged Kittiwake Red Deer Elephant Seal Man Scientific name Rissa tridactyla Cervus elaphus Mirounga augustirostris Homo sapiens Maximum lifetime reproductive output Male Female 26 28 24 14 100 8 888 32 Box 6.7. Maximum known lifetime production of offspring in several species according to their mating system. Modified from Krebs & Davies (1993). 6.3.2. Monogamy Monogamy is more typical of birds than of any other animal group. Up to 90% of bird species were thought to be monogamous prior to the employment of molecular analyses to determine paternity. However, as noted in Chapter 5, such monogamy is not so clear-cut when examined at a genetic level. Extra-pair copulations mean that some of the young in a nest have been fathered by a male other than the females social partner. Prior to drawing conclusions regarding the characteristics of monogamy we shall consider the case of the barn swallow (Hirundo rustica), a species that has been regarded as typically monogamous. This swallow is very well known thanks to the work of Anders Møller, of Pierre et Marie Curie University of Paris, France. The following account derives from Møller (1994). Early each spring, the swallows return to Europe from their African winter quarters to breed. As we noted in Chapter 4, the males have somewhat longer tail streamers than the females and these ornaments serve as indicators of their quality. The longer-tailed males arrive and find mates earlier. The early-arriving females are also of higher quality than those that follow. The longertailed males pair with the earlier females, which tend to be larger and are often capable of producing two broods per season. Long-tailed males tend to invest less on parental care and females paired with them tend to invest more on parental duties than do those paired with shorter-tailed males. Swallows are monogamous but this is not to say that they are faithful. Both males and females may mate with other than their regular partners, although not all individuals are equally successful in obtaining extra-pair copulations. Longer-tailed males are more successful in mating with other females but short-tailed males never do. Among females, those paired with short-tailed males are most likely to take part in extra-pair copulations but those paired with long-tailed mates hardly ever do so. In other words, the tail length of their males determines whether or not females have extra-pair copulations. This apart, instances of intraspecific nest parasitism sometimes occur, generally when there is a high density of breeding pairs. Here females lay some of their eggs in the nests of neighbours that have started laying at about the same time. The swallow example, which may be typical of most monogamous passerine birds, reveals some important matters, notably that avian monogamy is not based on mutual collaboration and fidelity, as some people used to like to believe. In accordance with intersexual conflict theory, the male and female do not have identical interests and individuals of each sex try to maximise its own reproductive success. This explains the existence of extra-pair copulations in males as a strategy for increasing the number of their offspring. Females take part in such copulations because, by mating with males of higher quality than their own, they too improve their reproductive success, not by producing more young but by raising young of higher quality. Females of many species have also developed intraspecific nest parasitism as a strategy that allows them to increase the number of offspring that they contribute to the next generation. Bearing in mind that a males own nest often holds young fathered by other males, we can also draw another conclusion, which we highlighted in Chapter 5, that it is necessary to distinguish between social monogamy (pair formation to raise progeny) and genetic monogamy (where all offspring are fathered by the incumbent male). The latter is much less common than was thought to be the case twenty years ago, given the frequency of extra-pair copulations (see Chapter 5). Social 69 monogamy is easily revealed but detecting genetic monogamy --which furthermore may be highly variable in occurrence between different populations of the same species-- requires molecular analyses. Thus, throughout this chapter, references to monogamy mean social monogamy, except where otherwise specified. The rarity of genetic monogamy is unsurprising given that each member of a pair strives to increase its own individual reproductive success and not that of the pair. When all is said and done, what may seem strange is that genetically monogamous species should exist at all, and they do! There are indeed species in which the partners pair for life and in which both males and females remain faithful to each other. This is seen particularly among some raptors, corvids and seabirds. A number of hypotheses have been offered to explain the evolutionary persistence of monogamy. In the above-mentioned groups, where such monogamy is widespread, the species tend to be long-lived and the males are considered to be indispensable for the care and feeding of the young. The males incubate, or feed the female while she does so, and later they bring about half of the food needed by the chicks during their development. Monogamy makes sense in species such as these where the needs of the young cannot be met by just one member of the pair and the collaboration of both is essential. This idea is supported by the fact that reproductive success in many of these species has been shown to increase over time, as the partners gain in experience. Another group of birds in which extreme parental care is necessary is the hornbills (family Bucerotidae), large-billed, often frugivorous, birds whose reproductive behaviour is unique. The female seals herself into a cleft in a tree trunk using mud initially and later faeces and food residues, leaving only a small hole for ventilation and for receiving food from the male. She lays her eggs and does not leave the hole until the fully-developed chicks are ready to fledge. She takes advantage of the opportunity to moult becoming naked and flightless during this time. Parental care is thus almost entirely the concern of the male and it is especially costly since he must feed the female throughout and after incubation as well as the chicks during the fledgling period. It is hard to understand why male hornbills are prepared to perform such an arduous task, but we can imagine two evolutionary scenarios that may explain it. Firstly, despite being incarcerated, the females must play an important part in ensuring the survival of the chicks. Also, monogamy in such species must be genetic, not just social, since natural selection would only favour such enormous investment in parental care by the male if it was for the benefit of his own young. Both predictions are fulfilled. The narrowing of the access hole by the female is highly effective defence against predation. Also, in some species at least, molecular investigation of paternity confirms that the females are entirely faithful and none of the chicks in hornbill nests are fathered by other males (Stanback et al. 2002). The earlier idea provided for explaining monogamy in hornbills would not be valid for many bird species in which the female alone is capable of raising at least part of her brood, nor does it apply to most species of other animal groups. We shall go on to consider two examples of monogamous mammals, members of a group in which monogamy is very rare. These will assist us in examining other possible hypotheses that explain monogamy and will pave the way for studying human mating systems. Campbells dwarf hamster (Phodopus campbelli) is a small monogamous rodent of the Russian steppes. Males take great interest in their offspring and offer all kinds of parental care, other than providing milk, which they cannot do. They even assist at birth, helping the young to emerge, cleaning them and eating the placentas (this is the only known mammal to do this). The male spends a great deal of time with the young in the burrow, which is very important since this hamster inhabits a very cold, dry habitat. They keep the young warm while the female emerges to find moist food. Monogamy and parental care by males are very rare in rodents. Even congeneric species, such as the Djungarian hamster (Phodopus sungorus) do not behave like Campbells dwarf hamster. The Djungarian hamster lives in less cold and dry areas, so that the female alone is capable of caring for the young (Wynne-Edwards 1995; Jones & Wynne-Edwards 2000). Marmosets and tamarins are very small American monkeys, many species of which are monogamous. The common marmoset (Callithrix jacchus), one of the beststudied species (Evans & Poole 1983; Albuquerque et al. 2001), lives in family groups composed of a male, a female and one or more young of various ages. The females generally give birth to twins, which are quite large at birth, around 23% of their mothers weight. The males play an active role in caring for the young, watching over them and, especially, carrying them. In this species monogamy once again seems to be based on the need for the males collaboration in raising the young but there are other factors that contribute to its maintenance. Females live widely separated, so there are few opportunities for males to meet other females. Also the females reproduce very rapidly (they can become pregnant again only 20 days after giving birth). In these circumstances, when a male finds a female, he probably benefits by staying with her in order to guard her against rival males. Monogamy is also favoured by the fact that both males and females are very aggressive towards any same-sex individuals who approach their group. In other words, both sexes enforce monogamy on their partner. These mammalian examples reveal that monogamy may evolve under specific ecological conditions. As in birds, it is important that there should be major benefits from parental care. Natural selection may favour monogamy if either sex cannot raise the young unaided. The latter example also allows us to offer another hypothesis that explains why monogamy exists. It may evolve when it is very hard for males to find females, either because these are widely separated from each other or because they are very well guarded by their males. Under such conditions the best option for a male is to remain with the first female he can acquire. 6.3.3. Polygyny This mating system in which one male pairs with several females (see Box 6.6) is the commonest in nature. It predominates in mammals, 97% of which are polygynous, but also in the great majority of other animal species. As we have observed, this is generally the most successful system for males but it is less ideal for females, so that inter-sexual conflict tends to be significant. Polygyny only occurs in species in which resource distribution enables a dominant male to 70 monopolise several females. Its occurrence is thus chiefly determined by the distribution of resources and of the females themselves. If resources are patchily distributed, it becomes possible for a male to defend a rich patch and thereafter to mate with those females that come to use the resources that he owns. In contrast, it is much harder for males to be polygynous if resources are highly scattered or are uniformly dispersed. The same applies to the distribution of females. If these live in groups, whether in a particular territory or tending to use predictable routes, it may become possible for a male to succeed in mating with several females. Such behaviour becomes much more difficult where females are widely dispersed. There are no grounds for believing that females will make polygynous mating easy for the males, since this mating system is less productive for females. We might rather predict that females will distribute themselves according to resource distribution, risks of predation and their own gregarious tendencies, without giving too much regard to where the males are located. In contrast, males will decide their movements and distribution on the basis of female location. This prediction has been established for several mammal species. For example, Johan Nelson, of Lund University, Sweden, performed a detailed experimental investigation into the effect of female distribution and density in the field vole (Microtus agrestis). Female voles were placed in individual cages with supplies of food and water. Each cage had a hole so that males could enter but the females were prevented from escaping by a plastic collar. This arrangement permitted the investigator to modify both the distribution and density of females within fenced circular enclosures of 1,000 m2. Four males, fitted with radio-transmitters so that they could easily be located, were released into each enclosure. As predicted, males distributed themselves according to the distribution of females. Also when female density was high the males maintained smaller home ranges (Nelson 1995). The vole example serves to illustrate the most common arrangement seen with poygyny. The females conduct their lives without any regard for the males, but the males distribute themselves according to the disposition of females. No pairs form and males do not offer any parental care. Variations on this pattern are widespread. For example, in polygynous birds a more or less enduring seasonal pairing may occur between a male and a female, with or without parental care by the male. When males do not help to care for the young, it is all the same to the female whether the mating arrangement is monogamous or polygamous as far as reproductive effort is concerned. However, where a male does assist with parental care he tends to dedicate all his efforts towards his first female while leaving any other mates to fend for themselves. In this case we must assume that being polygynous is costly for all but the favoured females. Why then, in species where males help with parental care, do some females pair with already paired males when bachelor males are available? Two answers to this question have been proposed (see Box 6.8). By way of an answer Verner (1964) proposed a model, later popularised by Orians (1969), known as the ``polygyny threshold model. It proposes that when a female chooses to pair with an already paired male instead of with an unpaired one, it is because the polygynous male has a high quality territory. This will enable her to raise more offspring than she would have done in the territory of the monogamous male despite her not receiving any assistance with parental care, which the latter male would provide. This model has not been found to have as wide an application as was first believed, but it has played an important role in our understanding of the evolution of polygyny and it has received considerable support from some studies on birds. Polygyny with males providing parental care - Based on resource defence: the `polygyny threshold model - Based on deception of females Polygyny without males providing parental care - Based on resource defence - Based on defence of females - Based on leks Box 6.8. Models explaining the existence of polygyny in species in which the males provide parental care, and mechanisms used by them to achieve polygyny in species in which they do not contribute to parental care. See text for more details. One of the best of these was an experimental study of the red-winged blackbird (Agelaius phoeniceus) by Stanislav Pribil and William Searcy, of Miami University, USA. Nesting success in this species generally depends on nests being sited over water, those over dry land usually being less successful. The quality of two adjacent territories was manipulated experimentally during the breeding season, in order to test the polygyny threshold model. In one territory of each pair, chosen at random, nest platforms were placed over water (the high quality territory) and a female was allowed to remain, so that the incumbent male remained paired. Nest platforms were placed over dry land in the other territory (the low quality territory) and any females paired with the territory owner were removed, so that he was now unpaired. Fourteen such territory pairs were studied. As the model predicted, in twelve cases (86%) the first female to arrive settled in the high quality territory of an already paired male. Only two females (14%) chose to settle in the low quality territory of an unpaired male (Pribil & Searcy 2001). Another reason why a female may prefer to pair with a polygynous male has to do with deception by the already paired male, which convinces the second or third female into believing that he is actually unpaired. Such deception has been reported in several species, but the best example remains the classic study of the pied flycatcher (Ficedula hypoleuca) by Rauno Alatalo and his co-workers of Uppsala University, Sweden. Courting males defend a suitable nest-cavity (a nestbox in the study population) and sing to attract females. Very often, once a male has paired and the female has laid her clutch, the male finds another suitable cavity and sings to attract a second female. The observers noted that these males did not choose a cavity near the first nest, but rather chose one some way off, some 200m away on average but over 3km away on occasion. Once the second female had completed her clutch, the male abandoned her to return to his first mate, whom he assisted in raising the chicks. The deceived second female was left to raise and feed her chicks all on her own and, as a result, she fledged fewer than a monogamous female would have done. However, the 71 first polygamous female, given her mates assistance, fledged about the same number of chicks as did monogamous females (Alatalo et al. 1981). Male deception is sometimes more blatant. The hen harrier (Circus cyaneus) is a polygynous raptor in which males may pair with up to five females. Deception by the males here consists of bringing frequent and significant nuptial gifts (prey items) to all the females that they court, indicating to them that they are good hunters and will bring much prey to the chicks (see Chapter 4). However, once the chicks have hatched the males no longer bring the same amount of food to each female. They mainly assist the first female with whom they paired. The second female gets less help and any others receive very little assistance (Simmons 1988). Three types of polygyny figure among those mating systems in which the males do not deliver parental care (see Box 6.8). The polygyny may be based on resource defence, on direct defense of group of females or via defense of a display territory at a lek, although the boundaries between these are not always sharp, as we shall see. A good strategy for mating with females, if the males are not going to help with parental care, is to defend some resource that the females need in order to breed successfully. This may be a territory, food or a breeding site, for example. A male who is capable of securing possession of such a resource will be able to mate with females that come to exploit it. Resourcebased polygyny is particularly common in the many mammal species in which males play no part in parental care. For example, in the puku (Kobus vardoni) and the topi (Damaliscus lunatus), two medium-sized antelopes, the distribution of females within the territories of various males is explicable in terms of grass quality, although there are two other influencing factors: the males physical characteristics and protection from predators (Balmford et al. 1992). Polygyny based on defending females is also very common in mammals. The gorilla (Gorilla gorilla) provides a typical example. It lives in by groups that contain one male, usually three or four females, and their offspring (Gatti et al. 2004). Male gorillas defend their females and this strategy is easily understood since they all feed on leaves and other abundant plant material, so that resource defence is pointless whereas females do live together in defendable units. It is not always so easy to decide whether or not an instance of polygyny is due to resource defence or to female defence. For example, in the northern elephant seal (Mirounga angustirostris) the males arrive at the breeding colony beaches ahead of the females and the largest of them defend stretches of beach, i.e. territories. Once the females arrive, these spread out across the area and territory-holding dominant males mate with them, while keeping other males away, i.e. they defend the females. This is one of the most polygynous species known, some males acquiring harems of up to 100 females (Baldi et al. 1996). The females role in polygynous mating systems has traditionally been seen as insignificant and the striking and often noisy competition between males has always been regarded as deciding who pairs with whom. It is important to realise that this need not be the case. Females often have a chance to choose the male with whom they mate. Moreover, in many species females may often move from one harem into another. In addition, it has been found that in the grey seal (Halichoerus grypus), a polygynous species in which males are much larger than females and compete for harems between themselves, in 30% of cases the young born to a particular mother in successive years have all been fathered by the same male, who is not necessarily the harem master (Amos et al. 1995). This means that despite a dominant male controlling his harem, a female may give preference to another male, the father of her pups in earlier years. The third polygynous system in situations where males do not offer parental care is neither based on resource defence nor on female defence. This is lek polygyny (see Box 6.9) in which groups of sexually active males await visits from sexually receptive females. Definition: A lek is a gathering of males that perform courtship displays to females that visit the lek seeking males with whom to mate. Lek polygyny is a rare but widespread mating system that has been described in groups as diverse as birds, mammals, insects, lizards, amphibians (where they are known as choruses) and fish. Characteristics: 1. Males defend small territories that do not contain any of the resources that the females need. 2. Males do not deliver any form of parental care. 3. Males only provide females with their gene-containing sperm. 4. Females have free access and may mate with whichever male they choose. 5. Lek males have enormously variable reproductive success. A few males fertilise nearly all the females and many males do not fertilise any at all. Evolution: Various models have been proposed to explain lekking. The chief ones are: 1. The hot-spot model: males gather at places that females very often visit. 2. The hotshot of supermale model: males gather around a very attractive male who may entice many females to come to or near his territory. 3. Female choice model: males are obliged to gather since females need to make comparisons between them. Males outside the lek are not visited by females. 4. Kin selection model (see Chapter 8): if males are related, the less attractive individuals will also join a lek since it helps to increase the number of females that visit and hence increases the reproductive success of relatives. Problems: 1 It is very hard to identify which male characteristics influence female choice. The characteristics responsible have not been identified at all for some species and there are disagreements regarding others. a. Female choice is highly complex and based on multiple male characteristics. b. Potentially the most important of such characteristics are: morphology (size, colour and other adornments such as tail length), intensity of display (comprising sounds and movements mainly), position and size of territory within the lek, dominance status and previous experience. `The lek paradox is a theoretical problem based on the following argument: if females always choose those males with the best developed features, natural selection will favour the alleles that increase success and will eliminate those that reduce it. The point comes when there will be no genetic variation for those characters among males and then selection by females would confer little or no genetic benefit. 2 Box 6.9. Lek polygyny. Definition, evolution and associated theoretical problems. The first lek species to have been studied in detail was the sage grouse (Centrocercus urophasianus). Male sage grouse have extremely showy plumage and other ornamentation and they perform highly elaborate displays. They gather at dawn and dusk during the breeding season in groups of sometimes more than 15 birds. Each defends a small territory aggressively preventing its neighbours from coming too close. Females visit the lek for two or three days before 72 deciding to copulate with one of the males (they only choose one for each breeding event). They very often pick the same male given that only a few males perform most of the fertilisations. One study observed 105 copulations and nearly half of these were performed by the same male. The next two males in the females order of preference were responsible for around 20% of the copulations each and the fourth male accounted for 10%. The remaining 5% of copulations were shared between the remaining males, six of whom did not mate at all (Wiley 1973). Clear distinctions between the three types of polygyny do not always exist. For example, some males of lek species instead defend larger territories away from the lek and others may not display any type of territoriality. Topis, the antelopes to which we referred above, sometimes defend very small territories and in that case constitute a lek. In several species males of different populations have been found to employ different strategies. For example, males of most populations of red deer (Cervus elaphus) defend harems of females but in some parts of Spain they defend food resources for females, whereas they have been known to form leks in Italy. Manipulating the environmental conditions experimentally has been shown to bring about a change from defending harems to defending resource-containing territories. Juan Carranza and his co-workers of Extremadura University, Spain, provided food in areas in which red deer stags defend harems. The change was immediate. That same day the hinds remained near the food for most of the time and two of the stags switched to defending those areas. Five other stags also switched to defending territories rather than groups of female during the next few days (Carranza et al. 1995). 6.3.4. Polyandry This mating system, in which a female pairs sexually with several males, either at the same time or sequentially, is regarded the rarest in nature. Social polyandry, in which a female associates with several males, has been reported in very few species. Although genetic polyandry, in which a females offspring have more than one father, is quite common (see Chapter 5), social polyandry is only known for a few bird species, and in a few mammals, such as the saddle-backed tamarin (Saguinus fuscicollis), whose family groups most often contain one female, two males and their offspring (Goldizen et al. 1999). Sequential polyandry is most usual in polyandrous birds, in which the male alone provides parental care. The female mates with one male, lays her clutch and leaves it in the care of that male while she departs to repeat the process with another male. Such classic polyandry is typical among several shorebird species of the family Charadriidae. In this group when one member of a pair deserts it is usually the female. In the spotted sandpiper (Actitis macularia), females may mate with up to four males in succession. This species, as with jacanas, shows `sex-role reversal (see Chapter 4); the females are larger and compete for males among themselves. An alternative termed `cooperative polyandry also occurs in birds but even less often. Here the females pair with several males at one time and the latter perform most parental care. An interesting example is the eclectus parrot (Eclectus roratus), in which each female may mate with up to seven males. Robert Heinsohn and his co-workers from the Australian National University have studied this species for several years. They found that the female defends a nest hole where she and the chicks are fed by the males. Males compete aggressively for females but sometimes successive copulations by different males occur without any squabbling between them. An eight-year molecular genetic analysis of eclectus broods has shown that the two young that normally comprise a brood usually share the same father, but different broods involving the same female are fathered by different males. Some males never get to be fathers at all (Heinsohn et al. 2007). The rarity of social polyandry has always been explained on the grounds of basic considerations that we have noted several times (see Chapter 4). In this case they are that females have little to gain by mating with more than one male and also that, in mammals and birds, the males always have the first opportunity to desert and so to leave the female caring for the young. Nevertheless, as indicated in Box 6.10, although copulating with several males does not increase a females reproductive success, she may obtain both direct benefits (to herself) and indirect ones (for her offspring). Social polyandry is certainly rare. Nevertheless, as noted earlier and in Chapter 5, studies based on genetic analyses reveal that genetic polyandry is much more frequent. A further good example of this is provided by two Australian workers, Phillip Byrne of Monash University and J. Scott Keogh of the Australian National University, with their work on a small amphibian, the brown toadlet (Pseudophryne bibronii). As often happens with fish, male toadlets build and defend nests in which females lay their eggs. Observation and genetic analysis has shown that the female toadlet distributes her eggs between the nests of up to eight males. This means that the mating system is polygynous from the males standpoint, but is polyandrous from that of the females (Byrne & Keogh 2009). 1. Direct benefits: those obtained by the female herself a. Fertilisation is assured. Copulating with more than one male avoids the risk that a male might be sterile. b. Extra food is obtained. Mating sometimes involves receiving nuptial gifts or nutrient-rich ejaculates. Either may help a female to produce more descendants. c. Obtaining more parental care by the male. Exchanging sex with males for parental duties may benefit the female since the additional help may allow her to raise more offspring. d. Avoiding harassment by males. Where such harassment is common (as in some ducks where a female may even be drowned as a result), it may be a good strategy to copulate with another male who may protect her, or even to accept the aggressor male rather than to resist futilely. Indirect (genetic) benefits: those obtained for her descendants a. Increasing the genetic diversity of the offspring. This increases the chances that some at least may survive. b. Achieving genetic complementarity. The availability of sperm from several males makes possible selection by cryptic female choice (selecting the best sperm, see Chapter 5) in which females may select the sperm that best complements their own genetic constitution. c. Obtaining genes that render the offspring more attractive, in accordance with Fishers runaway selection model (see Box 4.6). d. Obtaining the best genes for increasing the chances that the offspring will be good at surviving, competing and leaving descendants. 2. Box 6.10. Possible benefits that females may derive from mating with several males. After Birkhead (2007). 73 6.3.5. Polygynandry and promiscuity As defined in Box 6.6, these mating systems are characterised by individuals of both sexes mating with several or many of the opposite sex. Polygynandry involves parental care but promiscuity does not. In polygynandry not all individuals are involved in copulation at the same time but this is more usual in promiscuous systems, which tend to occur among species with external fertilisation. In many fish and in marine invertebrates, males and females may assemble in very large groups and when the time comes they all release their gametes into the water at the same time, so that fertilisation happens on a vast scale. Polygynandry is very rare. It is somewhat more frequent in mammals, especially among primates and rodents, but it is very uncommon in other groups. Smiths longspur (Calcarius pictus) is one of the very few bird species that employs polygynandry, in which females copulate with various males in turn during their fertile period, and a male may copulate with several females. Subsequently, the male longspurs collaborate in bringing food to the nests owned by females with whom they copulated. Interestingly, male longspurs have been shown to be capable of `calculating how many chicks in a nest may be theirs and they bring food to the nest in accordance with this estimate. What is truly remarkable is that the feeds brought by a male to a nest are more closely correlated with the number of chicks he has fathered (established by molecular analyses of paternity) than with the time he spent with the female during her fertile period (Briskie et al. 1998). On what can Smiths longspur males base such an exact calculation? We have yet to find out. 6.3.6. Conclusions on classifying mating systems Box 6.6 presents a traditional classification of mating systems and we have seen that polygyny has always been regarded as the most frequent arrangement. Nevertheless, evidence has been accumulating over recent years that females play a much greater part in mate choice than has normally been attributed to them. Most previous investigators were men and this is still the case, so it is not surprising that the issue has always been studied from a male viewpoint. We noted in Chapter 5 that extra-pair copulations are most often initiated by the females and also that they happen in most monogamous species. Thus, although 90% of bird species are considered monogamous, on a genetic level and from the females point of view they may be considered polyandrous, since several males may have fathered the young in a nest. Also, in polyandrous species, where the female is the sex that benefits from multiple mating, females have several males to help them care for their young. They are not necessarily satisfied with just a few partners and sometimes continue seeking more-attractive males who also will father some of their offspring. The superb fairy-wren (Malurus cyaneus) provides an extreme example. This small Australian passerine does form pairs but the commonest reproductive unit comprises a female, a dominant male and several subordinate males. Nevertheless, despite possessing a harem of males that will later collaborate in raising the chicks, the female often also copulates with the most attractive neighbouring male (see Chapter 5), so much so that on average 76% of the chicks in the nest have not been fathered by any of the males in her family (Mulder et al. 1994). What then happens in polygynous species, in which the prejudiced sex is supposed to be the female? A brief summary of an outstanding study of the great reed warbler (Acrocephalus arundinaceus) by Dennis Hasselquist and his co-workers of Lund University, Sweden, will help to provide an answer. This is a polygynous species in which females choose those males with the most diverse vocal repertoires (an honest indicator of male quality as noted in Chapter 4) and whose territories are most rich in resources. It is certainly the case that the male provides little help in caring for the young, but, does this mean that he is taking advantage of the females? Molecular analyses of paternity revealed that females have extra-pair copulations with males whose song is more elaborate than that of their own partner. Moreover, the survival of the chicks after fledging is related to the size of their fathers repertoire (Hasselquist et al. 2002). In short, females choose the male who can best provide a foodrich territory. If he is not one of the highest genetic quality, the female will copulate with others of higher quality who will pass their good genes on to her offspring --see also the blue tit (Cyanistes caeruleus) study in Chapter 5. From a genetic viewpoint, polygyny becomes polyandry if there is a high rate of extra-pair copulations by females. Evidently some of the concepts relating to mating systems need modifying. I agree with Marlene Zuk (2002) that nowadays we have more than enough information to know that what is observed on a social level rarely matches what is going on at a genetic level. The high frequency of extra-pair copulations means that the commonest mating system is in fact polyandry. The Australian toadlet mentioned above provided an example of a species thought to be typically polygynous, since each male pairs with several females that lay the eggs in his nest, but that has been found to be polyandrous from the females standpoint on the basis of the more precise information supplied by molecular analyses. However, we may still have to wait a while before revising the classification of mating systems on the basis of genetic analyses of paternity. This is because such analyses have as yet been performed on few species and also because significant differences sometimes exist between different populations of the same species. 6.3.7. Human mating systems This section heading is not an error. I have written `systems since one cannot speak of a sole mating system in the human species. Although monogamy predominates in our western industrialised societies, this is not the case among other cultures. As with other primates, our mating system is variable and flexible since, as we have seen, ecological conditions have very direct influences on such systems. The human species is no exception and, since we inhabit a great diversity of habitats across nearly the entire planet, instances of practically all possible mating systems have been described (see Box 6.6). Despite this diversity, we shall end the chapter by trying to determine which mating system may be considered more widespread among our species. 74 According to an analysis of a large number of ethnicities and non-western cultures, i.e. those not under the strong religious or state influences that so characterise our own civilisation, the majority of societies are polygynous (83.4%), although monogamy is also well represented (16.1%) while polyandry is quite unusual (0.5%) (Cartwright 2000). We shall consider the different mating systems in the reverse order to our earlier review, with a view to dealing last with the most interesting, monogamy. 6.3.7.1. Polygynandry and polyandry 6.3.7.2. Polygyny Polygynandry (see Box 6.6) is extremely rare in humans. Setting aside the social experiments of the hippie communes of the mid 20th century, it can only really be found among the Inuit, and then in a very particular form unlike that which we described for some bird and mammal species. Two Inuit couples may have a mutual arrangement to share hospitality and help that extends to sexual favours. When a man needs to leave his wife for a time and visits the igloo of the other couple they will not only provide accommodation and assistance, but also he will be allowed to have sex with the woman, a favour that is reciprocated. Long absences of this type are uncommon which means that cross-copulation between such `associated couples is also uncommon and the risk of extra-pair paternity is not very high. On the other hand, the arrangement confers very important benefits since under the harsh living conditions of the Arctic a spell of poor hunting could mean death and being able to count upon the help of another couple (and a second set of relatives) is of inestimable value in times of scarcity. Polyandry (see Box 6.6) is also very uncommon. It is only frequent among several Himalayan peoples. Interestingly, instances of polyandry have two points in common in all cultures where they occur: the land is resource-poor and the men who share a spouse are often brothers. These circumstances favour polyandry. On the one hand, polyandry occurs where living conditions are so poor that it is hard for one man alone to provide the resources needed to support a family and so collaboration between two men is what makes raising a child possible. Also, the fact that the two men are brothers diminishes the inevitable conflict associated with sharing the same woman. For example, in a Sri Lankan population in which such husbands were not always brothers, it was shown that the marriages were more stable and lasting when they were brothers than when they were not (Birkhead 2007). The older brother enjoys more frequent sexual relations so it is unsurprising that the younger one leaves to find a wife for himself when conditions permit. The joint occurrence of the above two circumstances in all cultures in which polyandry is practised supports the idea that it is an adaptation that strengthens social alliances that enhance reproductive success under difficult conditions. This adaptive conclusion has been criticised by some anthropologists but the evidence in favour of the hypothesis continues to accumulate (Smith 1998). Kim Hill and Magdalena Hurtado, of the University of New Mexico, USA, have described a special form of polyandry among the Aché, a huntergatherer people from Paraguay (Hill & Hurtado 1996). The men in this society are very violent and resolve problems by fighting with sticks, as a result of which Polygyny, as we have seen, is the most frequent mating system in cultures outside western influences. There is strong evidence that it has always been widespread. For example, numerous passages in the Bible make it clear that the Israelites, together with all other peoples of the region, allowed a man to have as many wives and concubines as he could support. The custom is so ancient that the first polygynous man mentioned is Lamec, son of a great-great-grandson of Caín, one of the sons of Adam and Eve (Schwartz 2008). As happens in other species and also in polyandry, polygyny is influenced by environmental factors (see Box 6.6). The relationship is a complex one. According to a review by Bobbi Low (2000), the factors that most influence polygyny are the risk of parasites, the seasonality of the rains, irrigated agriculture and hunting. Together these explain 46% of instances of human polygyny. The most surprising and interesting finding is that parasite abundance has the clearest effect. It has been often maintained that polygyny is chiefly determined by resource availability, as happens in other animals (see Box 6.8). The thinking is that monogamy would predominate when resources were scarce and polygyny would do so when they were abundant, for example in agricultural communities. However, the situation is far more complex and parasites instead appear to be especially important because, for example, monogamy is practically non-existent in areas with a high incidence of pathogens nor does polygyny involving marrying two sisters occur in those circumstances, unlike in other places where there are lower risks of contagion. According to Low (2000), both findings suggest that polygyny increases the genetic variability of offspring and would thus increase their resistance to parasites. However, the main advantage of polygyny is that it allows females to choose resistant mates (see Chapter 4). Lows review did not take account of another factor that has been shown to influence the spread of polygyny in humans: a shortage of men. It has been shown that polygynous trios often form after a war and these comprise a man and two sisters. The explanation is the same as that offered for polyandrous trios involving a woman and two brothers. The fact that the women are sisters reduces possible conflict among them. An interesting anecdote may help us to understand this situation. During our study of the black wheatear (Oenanthe leucura), which is covered fully in Chapter 2, we colour-ringed the adults at 200 nests but found only a single case of polygyny. Here there were two nests, ten metres apart, in one males territory, a rare event in what is usually a totally monogamous species. We noted that the two females were ringed and when we re-trapped some of them die. As a result, many children are orphaned and this considerably reduces their chances of survival, from 86% for children with a father to 50% for those without. The investigators found that Aché women tend to live with two men, one as the primary partner and another with whom sporadic sexual relations also occur, so that he too has a chance of fathering her children. They interpreted this hierarchical polyandry as an adaptive strategy that allows women to achieve protection for their children in the event that their first spouse dies. 75 them we found that they were sisters from the same nest. This helped explain the polygynous trio because normally one female would not tolerate a competitor for her partner. Normally one of the factors that impedes a male mating with two females is competition between the latter. Instead, as we saw in the case of the dunnock, each female will try to drive away the other so as not to have to share the parental care offered by the male. In this case, by being sisters the conflict was less and both accepted the situation. The same may happen among humans when few men are available. A woman might not accept her husband taking a second wife but, where that wife is her sister, it is less out of the question given the many genes shared by the two women. When speaking of human polygyny it is obligatory to give special attention to the famous harems that were a common feature of the palaces of sultans, emirs, kings, emperors and other rich and powerful leaders. Such extreme harems comprise a very recent phenomenon in human evolution. Until the development of agriculture made possible the accumulation of resources, it simply was impossible for a man to dispose of sufficient resources to be able to support several wives and their offspring. A review by Laura Betzig has revealed that harems were common among the great empires of antiquity such as Babylon, Egypt, India, China, the Incas and the Aztecs, and among all peoples ruled by powerful kings. The harems of King David and King Solomon are particularly renowned. All these men acquired great riches and so were able to collect many spouses, who provided them with a large number of children (Betzig 1986). We have already mentioned Moulay Ismael, emperor of Morocco from the late 17th century into the early 18th century, who had 888 children from his harem of some 500 wives (Box 6.7). Very probably the potentates of antiquity did even better since their harems were ever larger. The largest of all was perhaps that of King Solomon who, according to several sources, had 1,200 wives. Returning to the more usual type of polygyny, involving a man with two or just a few women, just as we did for animals in general we need to ask ourselves why a woman should pair with an already paired man. In our species, in which the man contributes to parental care, two models may serve to explain this, the polygyny threshold model and the mate deception model (Box 6.8). Does it benefit a women to be polygynous if the man disposes of abundant resources, as proposed by the polygyny threshold model? The answer is sometimes yes. A recent study by Mhairi Gibson and Ruth Mace, of Bristol University, UK, provides a good comparison between the reproductive success of a monogamous woman and that of a polygynous one. The number of children borne by a polygynous woman depends on her ranking within the mans spouses, as happens in birds. The first wife of a polygynous man has greater reproductive success than a monogamous woman but the second and third wives do less well, and this is reflected not so much in terms of the quantity of offspring but of their quality. The children of the second and third wives tend to be thinner, weighing less relative to their height, and so, probably having less chance of long life and high competitive ability (Gibson & Mace 2007). There are no detailed studies of the deception model but this mating system may have been quite common in situations where men had to travel in a regular fashion as in sailors having a wife in every port. Cases are still reported from time to time, especially now that information technology allows all those involved to keep in touch. For example, a recent news bulletin told of a lorry driver who was arrested for keeping two wives, each in a different Spanish city. Box 6.8 also gives three models that may explain polygyny in species in which the males do not participate in parental care, based on resource defence and female defence. Two possibilities are offered to explain why a woman might pair with an already-paired man in such circumstances: because she has decided that it is to her benefit or because she is obliged to do so, either by her own family or by the man himself. In both cases the men involved would probably have resources with which to pay the womans family. The other model of polygyny given in Box 6.8 is the lek model, in which males display to attract females. Does anything similar occur in humans? If you think about it, a discotheque offers certain similarities to a lek. Various women interact with various men and an exchange of information takes place via a diversity of displays. Instances of violence between the men in question are not unusual. However, two differences from leks proper arise. Copulation is not always being sought, some of the participants are seeking a pair-bonded partner. Also the females as well as the males advertise their attributes. This last is unsurprising since, as we noted in Chapter 4, since the human male also invests in parental care, he too is selective. 6.3.7.3 Monogamy This is the mating system of modern industrialised societies and, as we have seen, of 16.1% of traditional cultures. It is also always present among ethnicities in which polygyny or polyandry exist. Nevertheless, we must stress that monogamy in humans, as in other animals, does not imply fidelity. As we saw in Chapter 5, extra-pair copulations are also common in our species and these may result in children by other than the `official father. In other words, in the human species too, social monogamy does not always mean genetic monogamy. Monogamy may seem entirely normal to us, particularly if we live in a country where it is the only legal option, but in comparison with other species it is less usual. Only 3% of mammals are monogamous, so why are we among them? We have seen that one of the circumstances driving the evolution of monogamy is that the offspring require such demanding parental care that it is very hard for one parent to raise them alone. This situation applies to humans. Our babies are born highly dependent and incapable of doing anything for themselves. Their long period of dependency on their parents makes severe demands of the mother that make it almost indispensable for her to be able to count on the fathers assistance in order to raise them successfully. This is undoubtedly an important factor but it does not explain the differences that exist between ourselves and other primates since the females of our closest relatives also give birth to offspring that require a great deal of parental care, but they are not monogamous. The most widely accepted explanation (see the review by Buss 2007) is that the emergence of concealed ovulation in the human species is responsible for monogamy having become the most appropriate mating 76 system for our species, since it allows the woman to obtain more help with parental care and it provides the man with greater paternity certainty. The reasoning is as follows. Most female primates signal when they are in heat by changes in colour (and smell) and by swelling around the genital area. When males detect that females are in heat they can guard them and copulate with them during that period, deriving certain guarantees of paternity. At other times they can seek other females. When the females in one of our ancestral species ceased to signal when they were fertile and became potentially sexually available at all times, it became impossible for a man to guard a woman effectively, which thus enormously reduced his certainty of paternity. This left the man with two options. He could continue being polygynous, with the risk that when he was with one woman, another man could be with another of his wives, thus reducing his assurance of paternity. Alternatively, he could become monogamous and remain together with one woman, thus blocking access to her by other men and so increasing his paternity certainty. His chances of mating with other women would be reduced but he would have a greater chance of being the father of the children borne by his wife. It is also the case that the monogamous tendency would have been favoured by custom at a social and cultural level. Such rites have existed in all known cultures and they served to convert the union of a man and a woman into a publicly acknowledged and respected partnership. The impact of social norms, latterly including religion, became progressively stronger to the extent that monogamy is now imposed by law in many cultures. The idea that monogamy in the human species is an adaptive strategy that evolved long ago is supported by the fact that a mechanism exists that favours pair maintenance, and reduces the chances of extra-pair copulations: jealousy. This is a well established human adaptation, not only because it is common to all cultures, but also because it occurs in both males and females. Moreover, the factors that provoke jealously differ between the sexes in accordance with the predictions of evolutionary theory (see Chapter 5 for a detailed account of jealousy). 6.3.7.3.1 Is monogamy the typical mating system of industrialised countries? Having more than one spouse at a time is prohibited by law in western industrialised countries. This constitutes monogamy, from a social standpoint. However, from a biological point of view it is not so for two reasons. Firstly, the existence of extra-pair copulations implies a degree of polyandry. Secondly, monogamous unions are frequently broken by separation and divorce. Taking data supplied by the National Spanish Statistical Institute by way of example, 95,000­150,000 marriage dissolutions have occurred in my country annually over the past ten years, taking divorces and separations together. In total nearly 1,200,000 couples separated or divorced between 1998 and 2007, a very high number even without including the ever increasing but un-quantified number of unmarried couples that have separated unofficially. This high rate of relationship breakdown, which tends to be followed by the establishment of a new relationship (more often in men than in women) does not permit us to consider monogamy as typical of modern human societies. It is more accurate to speak of successive polygyny from the mans point of view or of successive polyandry from that of the woman. This phenomenon is also known as serial monogamy. 6.3.7.3.2. What is the typical human mating system from a biological viewpoint? This question can only be answered by reference to biological characteristics that are outside cultural influences. Two meet this requirement: sexual size dimorphism and relative testis size. With respect to the former, a number of comparative studies have shown a direct relationship between the degree of polygyny and sexual size dimorphism (the size difference between males and females of the same species). The more polygynous the species, the greater the sexual size dimorphism. The explanation lies in that a high level of polygyny implies greater competition between males so that sexual selection would favour the larger males. Sexual size dimorphism is moderate in humans, where a man is 8­10% taller and 20­40% heavier on average than a woman. This indicates that a moderate degree of polygyny would be typical of our species. Comparative studies support this conclusion. For example, according to data on anthropoid primates gathered by Cartwright (2000), sexual size dimorphism in polygynous species is greater than in other species. Thus, sexual size dimorphism expressed as male weight divided by female weight is 1.8 in the gorilla (Gorilla gorilla) and 2.2 in the orangoutan (Pongo pygmaeus), both of which are polygynous. In the polygynandrous chimpanzee (Pan troglodytes) it is 1.3 and in humans (Homo sapiens) it is 1.1. With respect to relative testis size, as we saw in Chapter 5, comparative studies have demonstrated that the greater the amount of sperm competition, the larger the testes. Harcourt et al. (1981) showed that human males fall between polygynous species such as the gorilla and polygynandrous ones such as the chimpanzee. In the gorilla, one male has several females and there is much inter-male competition but no sperm competition, whereas in the chimpanzee males and females live in groups so there is much sperm competition, but less direct inter-male competition. The data thus suggest that according to relative testis size the human mating system would be moderate polygyny with an also moderate level of sperm competition. Barret et al. (2002) provide additional evidence that supports the conclusion that moderate polygyny is the standard mating system of our own species. Monogamy has to be imposed by law in modern western societies in order to be maintained, although serial monogamy and other strategies can circumvent the law. 77 Chapter 7 Gregariousness, groups and societies 7.1. Introduction Nearly all animal taxa include some species whose individuals are solitary, pairing up only to reproduce, and others that form more or less substantial stable groups. These groups may simply be seasonal gatherings to achieve some objectives, such as attracting mates, or they may be permanent congregations within which all activities, such as food-seeking and reproduction, are performed. Gregarious species are those in which individuals form temporary groups in which they may or may not remain for long according to their interests. This in turn will depend on the balance between the costs and benefits of being in a group. In social species the relationship between individuals is generally tighter, social groups often being composed of relatives. Edward Wilson published his famous book `Sociobiology over 30 years ago. In it he defended the need to apply biological methods to the study of social behaviour in all species, including our own (Wilson 1975). The book stirred up enormous controversy, particular on account of its final chapter, which was devoted to the human species. Wilson was criticised not only as an inadequate scientist but also as an ideologue who was in effect defending racism, male dominance, social inequalities, genocide and rape, among other unpleasantnesses. These criticisms were rebutted in Chapter 1 of this book, precisely because I wish to justify, from a biological viewpoint, the joint study of human behaviour alongside that of all other animals. In the years after Willsons book was published, and although critics headed by Stephen Jay Gould did not cease their attacks, sociobiologists continued their evolutionary work, which helped explain a great many behavioural phenomena. After three decades of turmoil, history has pronounced its verdict: sociobiology has triumphed (see the book by John Alcock (2001) in which he applies lucid argument and crushing logic to justify this conclusion). Alcock (2001) highlights that whereas criticism did not impede the advance of sociobiology, it did harm the development of other social sciences, which have generally resisted the application of the theory of natural selection to an analysis of human behaviour, thanks to the criticisms of Gould and others. Sociobiologists on the other hand have made notable progress, not only in explaining the social behaviour of many species but also by discovering a great variety of strategies and behaviours that imply coordinated action by individuals in groups in species in which this had never been suspected. Thus, it has been shown that many microorganisms have quite complex social behaviour, which not only includes cooperation between individuals but also involves networks of communication that help them seek, reproduce and disperse (see a review by Crespi 2001). For example, Pseudomonas and other pathogenic bacteria have been shown to be capable of responding in unison in a coordinated way when it is necessary. They are able to communicate via certain molecules that they use as indicators of population density. This enables them to attack their hosts at the ideal moment, precisely when their population density has reached a level likely to maximize the success of individuals in reproducing or dispersing (Juhas et al. 2005). 7.2. The costs and benefits of living in a group Why are some species solitary and others gregarious or social? Before answering this question we shall examine what happens among spiders, a group that includes gregarious and solitary species, taking advantage of a review by Mary Whitehouse and Yael Lubin, of Ben Gurion University, Israel. There are approximately 38,000 known species of spiders and the great majority are solitary. Group living has been described for only some sixty species, 23 of which form fairly complex societies. In some cases gregarious species form large groups in which each spider builds its own web, captures its own prey and reprod