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Los Murciélagos De La Guayana Colombiana: Estructura De Comunidades Y Diversificación

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Los Murciélagos De La Guayana Colombiana: Estructura De Comunidades Y Diversificación Los murciélagos de la Guayana Colombiana: estructura de comunidades y diversificación Sebastián Cuadrado Ríos Universidad Nacional de Colombia Instituto de Genética Bogotá, Colombia 2020 I Los murciélagos de la Guayana Colombiana: estructura de comunidades y diversificación Sebastián Cuadrado Ríos Trabajo de investigación presentado como requisito parcial para optar al título de: Maestría en Ciencias - Biología Director: Mario Vargas-Ramírez Ph. D. Línea de Investigación: Biología Evolutiva Grupo de Investigación: Grupo de Biodiversidad y Conservación Genética Universidad Nacional de Colombia Instituto de Genética Bogotá, Colombia 2020 III V VI Murciélagos de la Guayana Colombiana A mis padres, Maria Elena y Einer, y Andrea Los pilares de este proceso Agradecimientos Agradezco a la Universidad Nacional de Colombia, y en particular a su Instituto de Genética, quienes me brindaron el espacio para desarrollar los experimentos de laboratorio que soportan esta tesis, y la posibilidad de pertenecer a una comunidad académica y estudiantil acogedora y altruista, que pronto me hizo sentir como en casa. Agradezco profundamente a mis colegas Hugo Mantilla, Darwin Morales y Olga Montenegro, quienes amablemente me confirieron los fragmentos de tejido que utilicé para el desarrollo de mi investigación. Agradezco a todos mis compañeros de grupo, con quienes compartí numerosas discusiones que nutrieron constantemente el desarrollo de este proceso, y me ofrecieron su ayuda cuando lo necesité. Mención especial para mi director, Mario Vargas Ramírez, quien me abrió las puertas para ingresar a su grupo de investigación, me brindó todas las herramientas que requería, y creyó en mí en todo momento; gracias a él esta tesis ha llegado a buen fin, y por ello le estaré profundamente agradecido. Agradezco a la Asociación Colombiana de Biología Evolutiva – COLEVOL, por el apoyo brindado a mi persona para la realización de esta tesis. Finalmente, agradezco a mi pareja, Andrea, y mis padres, Maria Elena y Einer, quienes me apoyaron en todo momento, creyeron en mí y dieron todo de sí para que cumpliera mis sueños. VII Resumen y Abstract IX Resumen Reconocer y entender patrones y procesos históricos que han influenciado la diversificación de los organismos sobre la tierra, es uno de los objetivos centrales de la biología evolutiva. Dentro de esta gran área, estudios enmarcados en las disciplinas de la sistemática molecular (i.e. filogeografía, filogenética y genética de poblaciones), nos permiten abordar preguntas evolutivas desde diferentes escalas biológicas, espaciales y temporales. La filogeografía y la filogenética molecular nos ayudan a entender aspectos relacionados con eventos que han dado lugar a patrones de variación genética de los organismos, así como entender el ensamblaje de comunidades biológicas en un área determinada. Este tipo de estudios aportan información crucial para aumentar el conocimiento acerca de biodiversidad de eco regiones poco estudiadas. Una de estas eco regiones es la Guyana colombiana. Esta eco región, la cual se encuentra ubicada entre tres centros putativos de especiación; Amazonía, Andes y Guayana, es una de las zonas menos exploradas del país. Como resultado de su composición geológica, los enclaves occidentales del escudo Guayanés han sido descritos como una "entidad heterogénea", compuesta de sabanas, catingas, bosques bajos, e inclusive bosques de arena blanca. Usando como grupo biológico de estudio los murciélagos, este trabajo de grado presentan dos aproximaciones enfocadas a entender como eventos biogeográficos que han moldeado la diversidad del continente, han afectado diferentes linajes que habitan la Guayana colombiana. Los murciélagos son un grupo de vertebrados sensibles a los eventos biogeográficos que han moldeado la diversidad del continente, el cuál cumple diferentes roles funcionales en los ecosistemas que habitan. Altos grados de asociación con el hábitat han sido descritos para numerosas especies de murciélagos, principalmente en cuanto a características de forrajeo y tipos de dieta. En un primer proyecto, analizamos comparativamente los patrones filogeográficos de tres especies de murciélagos de amplia distribución, con el objetivo de identificar los patrones de divergencia genética de los murciélagos que habitan el área en la actualidad. Utilizando secuencias de ADN mitocondrial, revelamos la existencia de poblaciones de murciélagos establecidas en el área, las cuales mostraron diferentes grados de flujo genético con áreas biogeográficas circundantes, en especial con las provincias guayanesas del Oriente y Pantepui y el Amazonas. Adicionalmente identificamos diferentes historias demográficas para cada especie, las cuales probablemente fueron influenciadas en diferente medida por cambios climáticos durante el pleistoceno y características ecológicas diferenciales. Nuestros resultados destacan la influencia de los ecosistemas guayaneses colombianos IX X Murciélagos de la Guayana Colombiana en la formación y configuración espacial de la diversidad y estructura genética en murciélagos, y la importancia de estos ecosistemas para la conservación dicha diversidad. En un segundo proyecto, desde una perspectiva filogenética, evaluamos la estructura filogenética de la comunidad de murciélagos de diferentes eco-regiones del norte de sur américa, usando secuencia de ADN mitocondrial y nuclear. Los resultados de los análisis nos permitieron demostrar que las poblaciones de murciélagos de la Provincia Guayanesa del Occidente (la cual incluye la porción colombiana del escudo guayanés), se encuentran filogenéticamente agregadas, es decir, las especies que componen las comunidades son más cercanas evolutivamente de lo esperado por el azar. Concluimos que factores como la alta heterogeneidad de hábitats en la región, la alta diversidad de murciélagos frugívoros en las comunidades muestreadas, y la competencia interespecífica han moldeado la composición de especies de las comunidades en esta zona. En un capítulo final, se desarrolla una discusión general de los resultados obtenidos de los dos proyectos de investigación realizados. Los capítulos uno y dos de esta tesis serán sometidos a revistas indexadas internacionales, razón por la cual están escritos en idioma inglés y en formato de artículo científico. Palabras clave: murciélagos, Guayana Colombiana, Provincia Guayanesa Occidental, filogeografía comparada, estructura filogenética de comunidades. Contenido XI Abstract Recognizing and understanding historical patterns and processes that have influenced the diversification of organisms on earth is one of the central goals of evolutionary biology. Within this broad area, studies within the disciplines of molecular systematics (i.e. phylogeography, phylogenetics and population genetics), allow us to address evolutionary questions from different biological, spatial and temporal scales. Phylogeography and molecular phylogenetics help us to understand aspects related to events that have given rise to patterns of genetic variation in organisms, as well as to understand the assembly of biological communities in a given area. These types of studies provide crucial information to increase knowledge about the biodiversity of little-studied ecoregions. One such ecoregion is Colombian Guyana. This ecoregion, which is located between three putative centers of speciation; Amazonia, the Andes and Guyana, is one of the least explored areas of the country. As a result of their geological composition, the western enclaves of the Guiana Shield have been described as a "heterogeneous entity", composed of savannas, catingas, lowland forests, and even white sand forests. Using bats as a biological study group, this paper presents two approaches focused on understanding how biogeographic events that have shaped the diversity of the continent have affected different lineages that inhabit Colombian Guiana. Bats are a group of vertebrates sensitive to biogeographic events that have shaped the diversity of the continent, which play different functional roles in the ecosystems they inhabit. High degrees of association with habitat have been described for numerous bat species, mainly in terms of foraging characteristics and diet types. XII Murciélagos de la Guayana Colombiana In a first project, we comparatively analyzed the phylogeographic patterns of three widely distributed bat species, with the aim of identifying the patterns of genetic divergence of the bats that inhabit the area today. Using mitochondrial DNA sequences, we revealed the existence of bat populations established in the area, which showed different degrees of gene flow with surrounding biogeographic areas, especially with the Guiana provinces of Oriente and Pantepui and the Amazon. Additionally, we identified different demographic histories for each species, which were probably influenced to different extents by climatic changes during the Pleistocene and differential ecological characteristics. Our results highlight the influence of Colombian Guiana ecosystems on the formation and spatial configuration of bat diversity and genetic structure, and the importance of these ecosystems for bat conservation. In a second project, from a phylogenetic perspective, we evaluated the phylogenetic structure of bat communities inhabiting different eco-regions of northern South America, using mitochondrial and nuclear DNA sequences. The results of the analysis allowed us to demonstrate that the bat populations of the Western Guayana Province (which includes the Colombian portion of the
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