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Ecological and Evolutionary Drivers of Chemical Communication Dynamics in Lizards

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Ecological and Evolutionary Drivers of Chemical Communication Dynamics in Lizards UNIVERSIDAD COMPLUTENSE DE MADRID FACULTAD DE CIENCIAS BIOLÓGICAS Departamento de Zoología y Antropología Física TESIS DOCTORAL Ecological and evolutionary drivers of chemical communication dynamics in lizards Factores ecológicos y de evolutivos que afectan a la dinámica de la comunicación química en lagartos MEMORIA PARA OPTAR AL GRADO DE DOCTOR PRESENTADA POR Roberto García Roa Directores José Martín Rueda Pilar López Martínez Madrid, 2017 © Roberto García Roa, 2017 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 2 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 3 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 FACULTAD DE CIENCIAS BIOLÓGICAS Departamento de Zoología y Antropología Física TESIS DOCTORAL Factores ecológicos y evolutivos que afectan a la dinámica de la comunicación química en lagartos (Ecological and evolutionary drivers of chemical communication dynamics in lizards) Memoria presentada por el licenciado Roberto García Roa para optar al grado de Doctor en Ciencias Biológicas, dirigida por el Doctor José Martín Rueda y la Doctora Pilar López Martínez del Departamento de Ecología Evolutiva del Museo Nacional de Ciencias Naturales- Consejo Superior de Investigaciones Científicas. Madrid, 2016 Roberto García Roa 1 2016 Ecological and evolutionary drivers of chemical communication dynamics in lizards © Roberto García-Roa, 2016 2 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 La foto que abre la sección general fue realizada por Roberto García-Roa. La ilustración antes de cada capítulo fue creada por Frutos García García. Queda prohibida la reproducción o publicación total o parcial, así como la producción de obras derivadas sin la autorización expresa de los autores. La presente Tesis Doctoral ha sido financiada por una beca predoctoral de Formación de Personal Investigador (FPI), BES-2012-054402, concedida por el Ministerio de Ciencia e Innovación. Asimismo, los estudios realizados han sido financiados por el Ministerio de Economía y Competitividad a través del proyecto CGL2011-23443 y CGL2014-53523-P. Todos los trabajos de investigación han sido respaldados por los permisos pertinentes. 3 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 4 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 FACULTAD DE CIENCIAS BIOLÓGICAS Departamento de Zoología y Antropología Física TESIS DOCTORAL Factores ecológicos y evolutivos que afectan a la dinámica de la comunicación química en lagartos (Ecological and evolutionary drivers of chemical communication dynamics in lizards) Memoria presentada por el licenciado Roberto García Roa para optar al grado de Doctor en Ciencias Biológicas, dirigida por el Doctor José Martín Rueda y la Doctora Pilar López Martínez del Departamento de Ecología Evolutiva del Museo Nacional de Ciencias Naturales- Consejo Superior de Investigaciones Científicas. Madrid, 2016 El doctorando Roberto García Roa V°B° del Director V°B° del Director V°B° del Tutor 5 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 José Martín Rueda Pilar López Martínez José A. Díaz 6 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 A todos los que creen que los sueños se pueden perseguir despiertos. 7 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 CONTENTS Contenidos ACKNOWLEDGEMENTS 10 Agradecimientos ABSTRACT 15 RESUMEN 19 INTRODUCTION 25 Introducción Objectives 47 Objetivos CHAPTERS: I: Semi-quantitative determination of scent compounds to analyse chemical signals of lizards 65 II: Genders matters: sexual differences in chemical signals of Liolaemus wiegmannii lizards (Iguania, Liolaemidae) 89 III: Diet constraints may restrict the expression of a potentially honest chemical sexual signal in Iberian rock 109 lizards IV: Interspecific differences in chemical composition of femoral gland secretions between two closely related wall lizard species, Podarcis bocagei and Podarcis carbonelli 135 V: Climatic Factors as Potential Drivers of interpopulational divergences in chemical signals of an Insular Lizard 141 8 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 V: Climatic factors as potential drivers of interpopulational divergences in chemical signals of an insular lizard 155 VI: Heterogeneous tempo and mode of evolutionary diversification of chemical compounds in lizard chemical signals 187 VII: The neglected scent of animal communication: a global analysis of the diversification of glands for chemical signaling in squamate reptiles 219 INTEGRATIVE DISCUSSION 251 Discusión general CONCLUSIONS 265 Conclusiones 9 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 AGRADECIMIENTOS /AGRADECIMIENTOS Dicen que para no perder la perspectiva de un camino es importante recordar su inicio y los pasos que cambiaron el rumbo del mismo. Esto es especialmente importante cuando el camino fue, es o será complicado. Tengo la suerte de conocer cada uno de los pasos que cambiaron el rumbo en mi camino y recordar, sin lugar a dudas, las personas que me acompañaron con sus consejos, ayuda o apoyo en esos cambios de etapa. Seguramente si le preguntan a alguien que me conozca dirá que todo empezó cuando era niño, momento en el cual sólo me gustaban los juguetes de animales y como siempre me recuerdan “cuanto más feos mejor”. Sin embargo, a nivel profesional, mi punto de inflexión fue Nicaragua. Allí tuve mi primer contacto con el trabajo de campo científico y seguramente es donde floreció (a nivel profesional) la parte más decidida de mí. Además, mi paso por Uruguay inundó mi cabeza de ciencia. Finalmente, mi segunda estancia en Nicaragua consolidó mi decisión mientras probaba mi fuerza de voluntad tanto física como mental. A continuación quiero agradecer personalmente cada una de esas personas que como decía antes cambiaron de alguna manera mi rumbo ayudándome a llegar a donde estoy ahora. Por conservar parte de mi intimidad daré solo sus nombres. En orden cronológico, Luisa M. Díaz Aranda (Universidad de Alcalá de Henares, España), Raúl Maneyro (Universidad de la República de Montevideo, Uruguay), Javier Sunyer (Universidad Nacional Autónoma de Nicaragua, Nicaragua) Jaime Bosch y Rafael Márquez (Museo Nacional de Ciencias Naturales-CSIC, España). Durante el trascurso de la tesis ha sido especialmente reveladora mi estancia con Daniel Pincheira-Donoso y Manuel Jara (University of Lincoln, United Kingdom), gracias por hacerme aprender tanto, gracias por encender una nueva luz en mi conocimiento. Desde Lincoln mi modo de entender la ciencia es diferente. Gracias por enseñarme que todo es posible, gracias por hacer equipo, gracias por confiar en mí, gracias familia. Muestra de nuestro trabajo juntos quedan dos capítulos de la tesis y ¡lo que queda por recorrer!. Thanks to Raoul Vandamme and Simon Baeckens (University of Antwerp, Belgium), my internship in Antwerp was an enriching, teaching and friendly experience. Thank you, it was an absolute pleasure for me. No me puedo olvidar de Ángel, Alfredo y Paco, Islas Chafarinas se quedará grabada en mí como un lugar de momentos únicos. Gracias, todos vosotros de una manera u otra me habéis ayudado en este camino. Gracias a las instalaciones de El Ventorrillo por acoger tantas ideas y trabajo. He de decir que durante estos años he conocido diferentes compañeros de trote en este camino profesional. Jesús Ortega, mi compañero y gran colega de profesión y pasión. Gracias por tus consejos dentro y fuera de la ciencia. Roger Colominas, Octavio Jiménez Robles, Diego Llusia, Rodrigo Megía-Palma, Juan Navarro y el resto de compañeros del museo, ha sido un placer contar con vosotros. Mis compañeros de grupo (aunque fuera por unos meses) Renata Kopena Alejandro Ibáñez y Gonzalo Rodríguez. Quién me diría cuando empecé el doctorado que iba a poder contar con la 10 Ecological and evolutionary drivers of chemical communication dynamics in lizards 2016 ayuda y apoyo de grandes profesionales como Emilio Civantos (Museo Nacional de Ciencias Naturales-CSIC, España), Salvador Herrando (Museo Nacional de Ciencias Naturales-CSIC, España), Shai Meiri (Tel Aviv University, Israel), Nuria Polo (Universidad Autónoma de Madrid, España) o Alfredo Salvador (Museo Nacional de Ciencias Naturales-CSIC, España), y de todas esas personas que dentro y fuera del museo me han ayudado de una manera u otra. En lo personal (y desde luego profesional) quiero dar las gracias de manera especial a mi gran amigo Santiago Carreira. No olvidaré aquel e-mail en el que te pedí consejo sobre mi segunda estancia en Nicaragua. Yo era estudiante y demasiado joven, tenía que organizar un viaje en una zona inexplorada con minas anti-persona y arenas movedizas (literal). Me diste consejo y apoyo, y eso no ha cambiado con el tiempo. Hay pocas personas con las que sientes aprender en cada momento. Puedo decir con orgullo que una de ellas es Santiago Carreira. Gracias, espero por mucho tiempo poder seguir aprendiendo de ti. He dejado para el final el agradecimiento a mis jefes, supervisores y colegas José Martín y Pilar López, ellos me han dado la oportunidad de dar uno de los pasos más importantes en el camino de la ciencia, formarme como investigador y adentrarme en el mundo de la ecología. Además, me habéis ayudado con esta oportunidad a vivir la
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