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Universidad Michoacana De San Nicolás De Hidalgo UNIVERSIDAD MICHOACANA DE SAN NICOLÁS DE HIDALGO FACULTAD DE BIOLOGÍA PROGRAMA INSTITUCIONAL DE DOCTORADO EN CIENCIAS BIOLÓGICAS OPCIÓN: CONSERVACIÓN Y MANEJO DE RECURSOS NATURALES PATRONES FILOGEOGRÁFICOS EN PECES VIVÍPAROS DISTRIBUIDOS EN EL CENTRO DE MÉXICO TESIS QUE PARA OBTENER EL GRADO DE DOCTORA EN CIENCIAS BIOLÓGICAS Presenta M. en C. Rosa Gabriela Beltrán López Director de Tesis Dr. Omar Domínguez Domínguez Morelia, Michoacán. Septiembre de 2018. AGRADECIMIENTOS A mi director de tesis, el Dr. Omar Domínguez Domínguez por todo el apoyo recibido durante estos cuatro años, por darme total libertad, respaldo y confianza para llevar a cabo el proyecto ahora culmidado, y por impulsarme siempre a ser mejor y esforzarme más. Al Dr. Ignacio Doadrio, por que aunque no tiene el título de Director de tesis, también lo fue, gracias por hacerme sentir como en mi casa el tiempo que estuve en el Museo Nacional de Ciencias Naturales, gracias también por darme total libertad de decisión y por abrirme las puertas de su laboratorio. A mi comité tutoral: Dra. Sabina Irene Lara Cabrera, Dr. Antonio González Rodríguez y el Dr. Miguel Martínes Trujillo, por sus valiosos comentarios y correcciones durante este proceso, por que cuando proponíamos un nuevo capítulo, nunca dijeron que no, siempre tuvieron total confianza en mi, gracias por todo. Al Dr. Rodolfo Pérez Rodríguez, por sus valiosos y acertados comentarios siempre que me sentía pérdida en algún capítulo, por la paciencia para escuchar y apoyarme, gracias. A todos mis compañeros del laboratorio de Biología Acuática de la UMSNH, que siempre estuvieron presentes y que cuando algo me salía mal, siempre fueron los primeros en escucharme, además de todas las cosas divertidas y a veces nada divertidas que nos ha tocado vivir juntos, gracias por todo. A la Universidad Autónoma del Estado de Morelos, el Centro de Investigaciones Biológicas y los integrantes del Laboratorio de Ictiología, por su total apoyo a este proyecto, por darme la oportunidad de llevarlo a cabo. A las personas que integran el despacho del Dr. Doadrio y también algunos chicos de otros despachos, por que sin su ayuda y sin su amistad, me habría sentido pérdida en su país, muchas gracias por todos los momentos y por todo el apoyo, por mostrarme las cosas bellas de su país, espero que en algún momento de la vida podamos volver a coincidir. A todos mis amigos que han seguido esta historia de cuatro años junto a mi, muchas gracias por existir en mi vida A Conacyt por otorgarme la beca de Doctorado y beca mixta que hicieron posible estos estudios y mis estancias de investigación. Finalmente, y no menos importante, a mi familia, a quien les agradezco profundamente que caminen conmigo de la mano, que cuando me caigo, siempre están para levantarme, y cuando soy féliz están ahí para compartir esa felicidad, sin ustedes, antes de empezar este proyecto habría renunciado, pero ustedes no lo permitieron, gracias por existir. ÍNDICE RESUMEN 1 PALABRAS CLAVE 2 ABSTRACT 2 I. INTRODUCCIÓN GENERAL 4 II. OBJETIVOS 19 III. RESULTADOS 21 CAPÍTULO I 21 Phylogeny and taxonomy of the genus Ilyodon Eigenmann, 1907 (Teleostei: Goodeidae), base on mitochondrial and nuclear DNA sequences. CAPÍTULO II 77 Genetic differentiation among populations of the freshwater fish Goodea atripinnis Jordan, 1880 (Cyprinodontiformes: Goodeidae), implications for its evolutionary history and its taxonomy. CAPÍTULO III 113 Processes determining the cladogenetic events among populations of Xenotoca variata (Bean, 1887) (Cyprinodontiformes: Goodeidae). CAPÍTULO IV 166 Evolving in the highlands: the case of the Neotropical Lerma live-bearing Poeciliopsis infans (Woolman, 1894) (Cyprinodontiformes: Poeciliidae) in Central Mexico. IV. DISCUSIÓN GENERAL 238 V CONCLUSIONES 248 RESUMEN La actividad volcánica y tectónica de placas desde el Mioceno y los ciclos glaciales e interglaciares durante el Plioceno y el Pleistoceno, son los principales eventos que han moldeado la distribución geográfica de la variación genética en varios taxa de peces de agua dulce del centro de México. En la presente tesis, se usaron marcadores mitocondriales (cytb, coxI y dloop) y nucleares (S7, RAG1, RHO y B-ACT) con enfoque filogenético, filogeográfico y de genética de poblaciones para inferir la historia evolutiva de las especies de peces vivíparos; Xenotoca variata, Goodea spp. (especies de importancia económico cultural purépecha), Ilyodon spp. (Goodeidae) y Poeciliopsis infans (Poeciliidae), a lo largo de su área de distribución en el centro de México. Los resultados muestran patrones filogeográficos contrastantes entre las especies analizadas. Las especies de Xenotoca variata, Poeciliopsis infans e Ilyodon spp., tienen historias evolutivas y biogeográficas complejas, y están fuertemente ligadas a la intensa actividad volcánica y tectónica durante el Plioceno y el Pleistoceno y a los ciclos glaciales-interglaciares durante el cuaternario. Para estas especies se encontró una fuerte estructura genética y alta diferenciación genética entre los linajes obtenidos, que puede estar ligada a la configuración antigua de las cuencas hidrológicas y no a la configuración actual. Debido a los linajes divergentes encontrados, se recomienda el rePoeciliopsis infans y Xenotoca variata es necesario realizar una revisión taxonómica por la probable presencia de especies taxonómicamente crípticas. En el presente trabajo se mostró que las características ecológicas y biológicas propias de cada especie, juegan un papel importante en la estructuración genética de las poblaciones, permitiendo en algunas la diferenciación genética, mientras que en otros casos, la homogeinización genética entre las poblaciones, como es el caso de Goodea atripinnis, la especie más ampliamente distribuida en las cuencas hidrológicas del centro de México. Se encontró baja diferenciación genética entre todas las poblaciones y haplotipos compartidos por varias regiones biogeográficas. Este patrón sugiere colonización reciente hacia la mayor parte de las cuencas hidrológicas donde la especie se distribuye, debido a su alta capacidad de dispersión y a que es una especie muy abundante y tolerante a los cambios ambientales. Se ha 1 reconocido que las especies sexualmente monomórficas generalmente presentan baja diferenciación genética entre las poblaciones debido a que no existe selección sexual fuerte como en las especies dimórficas. Además, para esta especie, la dispersión mediada por humanos es posible debido a que es de importancia para consumo humano desde el establecimiento de la cultura Purépecha (ca. 3000 años). En el presente trabajo, se mostró que además de la historia geológica del centro de México, las características biológicas y ecológicas de cada especie determinan el patrón filogeográfico encontrado, se encontraron resultados contrastantes entre las especies estudiadas; indicando que la historia geológica de la región en conjunto con las características biológicas y ecológicas propias de cada especie han moldeado la historia filogeográfica de cada una de estas de manera diferente. PALABRAS CLAVE: Goodeinae, Poeciliinae, endémicos, Historia geológica, estructura genética ABSTRACT Volcanic and tectonic plates activities from the Miocene and glacial and interglacial cycles during the Pliocene and Pleistocene, are the main events that have shaped the geographic distribution of genetic variation in several taxa of freshwater fishes in central Mexico. In the present dissertation, we use mitochondrial (cytb, coxI y dloop) and nuclear markers (S7, RAG1, RHO y B- ACT) with phylogenetic, phylogeographic and population genetics frameworks to elucidate the evolutionary history of viviparous fish species Xenotoca variata, Goodea spp. (species of cultural and economic importance for the Purepecha culture), Ilyodon spp. (Goodeidae) and Poeciliopsis infans (Poeciliidae), along their distribution range in central Mexico. The results showed contrasting phylogeographic patterns among the analysed species. For the Xenotoca variata, Poeciliopsis infans and Ilyodon spp their evolutionary and biogeographical histories are complex, and strongly linked to the intense volcanic and tectonic activities during the Pliocene and Pleistocene and to Quaternary glacial-interglacial climate change. For these species we found strong genetic structure and high genetic differentiation between lineages that 2 could be linked to the ancient configuration of the hydrological Basins and not it's the current configuration. Due to the divergent lineages found, we encourage the rearrangement of the current taxonomic status for Ilyodon species, while Poeciliopsis infans and Xenotoca variata require a taxonomic review, given the probable existence of cryptic species. We showed that the ecological and biological characteristics of each species played an important role in the genetic structure of populations, allowing in some cases genetic differentiation, while in other cases, genetic homogenization between populations, as is the case of Goodea atripinnis, the most widely distributed species in the hydrological Basins of Central Mexico. Low genetic differentiation between all populations was found and shared haplotypes for several biogeographic regions. This pattern suggests a recent colonization towards most of the hydrological Basin where the species is distributed, due to the high dispersal capacity, its high abundance and its tolerance to environment changes. It has been recognized that sexually monomorphic species usually have low genetic differentiation among populations
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