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UNRAVELING the CONTRIBUTION of CLIMATIC HETEROGENEITY on EVOLUTIONARY PROCESSES WITHIN OOPHAGA POISON DART FROGS Diana María G

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UNRAVELING the CONTRIBUTION of CLIMATIC HETEROGENEITY on EVOLUTIONARY PROCESSES WITHIN OOPHAGA POISON DART FROGS Diana María G UNRAVELING THE CONTRIBUTION OF CLIMATIC HETEROGENEITY ON EVOLUTIONARY PROCESSES WITHIN OOPHAGA POISON DART FROGS Diana María Galindo-Uribe Grupo de Ecofisiología, Comportamiento y Herpetología-GECOH Departamento de Ciencias Biológicas Universidad de los Andes Bogotá, Colombia TESIS SOMETIDA AL DEPARTAMENTO CIENCIAS BIOLÓGICAS EN EL CUMPLIMIENTO PARCIAL DE LOS REQUISITOS PARA OBTENER EL GRADO DE DOCTOR EN CIENCIAS - BIOLOGÍA Tutor Adolfo Amézquita, PhD Universidad de los Andes UNIVERSIDAD DE LOS ANDES BOGOTÁ, COLOMBIA Febrero 2017 TABLE OF CONTENTS ACKNOWLEDGMENTS ....................................................................................... III ABSTRACT ............................................................................................................. 1 RESUMEN ............................................................................................................... 2 GENERAL INTRODUCTION ................................................................................. 4 COLOUR AND PATTERN VARIATION AND PLEISTOCENE PHYLOGEOGRAPHIC ORIGIN OF THE STRAWBERRY POISON FROG, OOPHAGA PUMILIO, IN NICARAGUA .............................................................. 21 THE ROLE OF CLIMATIC SEASONALITY AND UNPREDICTABILITY IN SHAPING INTERSPECIFIC PATTERNS OF GEOGRAPHIC VARIATION IN WATER BALANCE TRAITS OF DENDROBATES AND OOPHAGA SPECIES ..... 44 THE SENSITIVITY OF LOCOMOTOR PERFORMANCE TO DEHYDRATION IN THE POISON FROG OOPHAGA PUMILIO (ANURA, DENDROBATIDAE) ............... 79 DOES FINER ENVIRONMENTAL HETEROGENEITY PROMOTE MICROEVOLUTIONARY PROCESSES? A CASE STUDY IN THE KÓKÓE-PÁ POISON FROG, OOPHAGA HISTRIONICA, IN COLOMBIA ............................. 91 CONCLUSIONS .................................................................................................. 122 ii ACKNOWLEDGMENTS Quisiera Agradecer a mi tutor Adolfo Amézquita por todos estos años de invaluables enseñanzas académicas, pero sobre todo por haberme enseñado otra forma de estudiar la vida y las ranas. También por su apoyo personal sin el cual no habría sido posible terminar mi doctorado. Quisiera agradecer a Heike Pröhl por su gran apoyo logístico, académico y personal en el desarrollo de diferentes capítulos de esta investigación. A Catalina Gonzales por su gran disposición y comentarios personales que contribuyeron enormemente a este trabajo. A Carlos Navas y Daniel Cadena por anteriores evaluaciones y valiosos comentarios a mi proyecto. A los diferentes investigadores que participaron y apoyaron la realización de esta tesis: Miguel Vences, Santiago Merino, Santiago Ron y Susane Hauswaldt. A mis amigos herpetólogos que también participaron de esta investigación y me han apoyado en diferentes etapas: Abel Batista, Jose Alfredo Hernandez, Fernando Vargas, Roberto Marquez e Iliana Medina. A mis amigos de la Universidad de los Andes y del laboratorio GECOH que me han apoyado y aportado en este proceso: Valeria Gonzalez, Javier Mendez, Carolina Esquivel, Mieidy Betancourt, Pablo Palacios, Beatriz Eugenia Velasquez, Catalina Silva, Osvaldo Gil, Vicky Felchas, Nelsy Pinto e Ivan Beltrán. A mis amigos técnicos y estudiantes en el Instituto de Medinica Veterinaria de Hannover que me apoyaron en la pasantía: Sabine Sippel, Johara Brooke, Corinna Dreher y Constantine. A Federico Chinchilla, Alejandro Farji y al curso más Zombie. A Colciencias, la Facultad de Ciencias de la Universidad de los Andes, la Organización de Estudios tropicales y a la DGTH por financiar mis estudios y proyectos. A la Universidad de Medicina Veterinaria de Hannover, A la Pontificia Universidad Católica de Ecuador, A la Universidad Nacional Autónoma de Nicaragua. Al Ministerio de Medio Ambiente y Desarrollo Sostenible de Colombia, al Ministerio del Ambiente y los Recursos Naturales de Nicaragua, Al Ministerio de Ambiente de Panamá, Al ministerio de Ambiente de Costa Rica por los permisos de investigación otorgados. iii Quisiera agradecer a mis profesores de pregrado y anteriores investigaciones que han aportado en mi vida académica y personal: Julio Mario Hoyos, Saúl Prada, Carlos Rivera y Alberto Acosta. A las ranas, bosques, paisajes y personas que inspiraron este trabajo y me regalaron a mi esposo Javier e hijo Pablo. A mi esposo quiero agradecerle por haberme apoyado, enseñado y participado como herpetólogo, amigo y compañero en todo este proceso. A mi hijo, quien fue el mejor resultado de mi tesis, por darle relevancia y un mejor sentido a mis quehaceres. A todos ellos gracias por su apoyo a paciencia. A mi madre por ser una gran mujer, mi mejor ejemplo a seguir y por su apoyo incondicional a lo largo de mi vida. A todos ellos quisiera finalmente dedicarles este trabajo. Porque este es gracias a ellos y para ellos. iv ABSTRACT Understanding the role of climatic factors on diversification processes remains among the pivotal questions in ecology and evolutionary biology. The main goal of this study was to approach this question at different temporal and spatial scales within a convenient model: the egg-feeding poison frogs in the genus Oophaga and their relatives. I first constructed a phylogeographic hypothesis on the evolution of Oophaga pumilio lineage. Phylogeographic analysis suggest that the Nicaraguan populations originated by a Late Pleistocene range expansion northwards, and reconstructs the origin of the species in southeastern Costa Rica. I investigated geographic variation in physiological traits linked to the regulation of evaporative water loss and tested for correlations with current and past climatic heterogeneity. I further assessed the effect of dehydration on the locomotor performance of Oophaga pumilio. Both temporal and spatial heterogeneity in climate contributed to explain geographic variation in evaporative water loss and body size; and the rates of water loss in frogs had a negative effect on their locomotor performance, eventually affecting the survivorship and fitness of individuals. Finally, to test for the role of microclimatic heterogeneity in shaping dispersal mechanisms and promoting microevolutionary processes, I studied the contribution of local variation in microclimate, topography and availability of reproductive resources in shaping the distributional patterns of individuals, and gene flow and genetic structuring within a population of Ooophaga histrionica. I conclude that climatic heterogeneity was correlated with phenotypic and genotypic divergence in Oophaga frogs at different spatial and temporal scales. Local environmental heterogeneity affected the distribution of individuals and the gene flow among spatial clusters of reproductively active individuals. Combining my data and previous studies, the evidence supports that climatic heterogeneity acted in conjunction with sexual selection and predation processes as the main factors promoting evolutionary divergence within this genus. 1 RESUMEN Una de las preguntas más esenciales en ecología y biología evolutiva ha sido entender el rol de factores climáticos en procesos de diversificación. El objetivo principal de este estudio fue abordar esta pregunta a diferentes escalas temporales y espaciales en un modelo convencional: las ranitas comedoras de huevos del género Oophaga y sus parientes. Inicialmente reconstruí una hipótesis filogeográfica acerca de la evolución de Oophaga pumilio incluyendo poblaciones de Nicaragua no incluidas en estudios preliminares. Los análisis filogeográficos sugieren que estas poblaciones se orignaron a través de la expansión de su rango de distribución al norte durante el Pleistoceno tardío y reconstruyen el origen de la especie en el suroccidente de Costa Rica. Posteriormente investigué la variación geográfica en rasgos fisiológicos relacionados con la regulación de pérdida de agua por evapotranspiración y puse a prueba correlaciones entre estos rasgos fisiológicos con las condiciones de heterogeneidad climática temporal. Concluyo que la heterogeneidad climática contribuye a explicar la variación geográfica en la pérdida de agua por evapotranspiración y el tamaño corporal. Posteriormente evalué el efecto de la deshidratación en el desempeño locomotor. Finalmente, para poner a prueba la contribución de la heterogeneidad microclimática en moldear los procesos de dispersión local y promover procesos microevolutivos, estudié la contribución de la heterogeneidad del clima local, la topografía y la disponibilidad del recurso reproductivo sobre la distribución espacial de los individuos, el flujo genético y la estructura genética dentro de una población de Oophaga histrionica. La heterogeneidad ambiental local afectó la distribución de los individuos y el flujo genético entre clusters espaciales, compuestos de individuos activos reproductivamente. A partir de la combinación de mis datos y de estudios previos, la evidencia soporta que la heterogeneidad climática actúa en conjunto con la selección sexual y procesos de depredación, como los principales factores promoviendo divergencia evolutiva al interior del género. 2 Oophaga pumilio from Río Indio Lodge, Nicaragua. 3 GENERAL INTRODUCTION Environmental and historical factors seem to act in conjunction, along current and evolutionary time scales, in shaping the dispersal of lineages and the diversity patterns of assemblages and communities across geographic gradients. Contemporary factors include ecophysiological performance, competition, habitat diversity and habitat choice. Historical factors include evolutionary and biogeographical processes that lead to transformation: the temporal dynamics of the distribution
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