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Taxonomy of the Genus Brachyteles Spix, 1823 and Its Phylogenetic

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Taxonomy of the Genus Brachyteles Spix, 1823 and Its Phylogenetic MUSEU DE ZOOLOGIA DA UNIVERSIDADE DE SÃO PAULO Taxonomy of the genus Brachyteles Spix, 1823 and its phylogenetic position within the subfamily Atelinae Gray, 1825 José Eduardo Serrano Villavicencio São Paulo 2016 MUSEU DE ZOOLOGIA DA UNIVERSIDADE DE SÃO PAULO MASTOZOOLOGIA JOSÉ EDUARDO SERRANO VILLAVICENCIO Taxonomy of the genus Brachyteles Spix, 1823 and its phylogenetic position within the subfamily Atelinae Gray, 1825 Dissertação apresentada ao programa de Pós-Graduação do Museu de Zoologia da universidade de São Paulo para o obtenção de titulo de Mestre em Sistemática, Taxonomia Animal e Biodiversidade Orientador: Prof. Dr. Mario de Vivo São Paulo 2016 Ficha catalográfica Serrano-Villavicencio, José Eduardo Taxonomy of the genus Brachyteles Spix, 1823 and its phylogenetic position within the subfamily Atelinae Gray, 1825; orientador Mario de Vivo. – São Paulo, SP: 2016. 198 p.; 56 figs; 10 tabs. Dissertação (Mestrado) – Programa de Pós-graduação em Sistemática, Taxonomia Animal e Biodiversidade, Museu de Zoologia, Universidade de São Paulo, 2016. 1. Brachyteles, 2. Filogenia - Brachyteles, 3. Atelinae I. Vivo, Mario de. II. Título. Banca Examinadora _______________________________ ___________________________ Prof. Dr. Prof. Dr. Instituição: Instituição: Julgamento Julgamento: _______________________________ Prof. Dr. Mario de Vivo (Orientador) Museu de Zoologia da Universidade de São Paulo ©Stephen Nash Con todo mi amor para Elisa y Juan que son mi razón para jamás desistir. Nunca terminaré de agradecer cada uno de sus sacrificios. Agradecimentos Aunque la gran mayoría del presente trabajo se encuentra redactado en inglés, quise tomarme la libertad de expresar mis agradecimientos más sinceros en mi lengua materna para no dejar ningún sentimiento al aire. En primer lugar, me gustaría agradecer a mi orientador Mario de Vivo quien se arriesgó a aceptar un desconocido biólogo peruano sin mayor experiencia. Fue gracias a nuestras conversaciones y discusiones que se despertó el sentido crítico que ahora poseo y que lastimosamente no es más común entre científicos. Gracias por las enseñanzas y por la oportunidad Mario. Me gustaría agradecer también a Marta Maria, Omair e Sônia del servicio de secretaria de posgrado y, al mismo tiempo, pedirles disculpas por las incontables veces que los incomodé. Gracias por todas las respuestas amables y soluciones rápidas que le dieron mis problemas. A Juliana Gualda, técnica de la sección de mamíferos del MZUSP, por la amistad y toda la ayuda ofrecida desde mi llegada. También a Ismael P. de Jesus, quien siempre se encontró dispuesto a ayudarme y a tener una buena conversación acompañada de un buen café. A los bibliotecarios del MZUSP, Dione Seripierri, Marta Zamana y Ricardo. Como buenos nunca desisten en la búsqueda de la bibliografía más extraña que se les presente. Su apoyo fue invaluable para hallar las referencias más difíciles que encontré. Al Dr. João Alves Oliveira y a Sergio M. Vaz del MNRJ por permitir el acceso a los especímenes depositados en esta institución. A Sergio M. Vaz nuevamente por enviarme sin demora la información de los especímenes depositados en el MNRJ. Al Dr. Castor Cartelle y al personal del laboratorio de Paleontología de la PUC–Minas, a Claudia Guimarães Costa del laboratorio de mastozoología de la PUC–Minas, por permitirme amablemente revisar material que fue de gran importancia para el presente trabajo. A Alexander Bibl y Frank Zachos del Natural History Museum of Vienna; Jacques Cuisin y Cécile Callou del Muséum National D‟Histoire Naturelle de Paris y Pepijn kamminga del Rijksmuseum van Natuurlijke Historie de Leiden por la cesión de fotos del material tipo y por la siempre rápida respuesta ante mis dudas. Al Dr. Fernando Perini y al personal del laboratorio de mastozoología de la UFMG por las facilidades y el apoyo brindado durante mi visita en su colección. A todo el lindo grupo que trabaja en la colección de mamíferos del Museo de Biología Mello Leitão, especialmente a Juliana Paulo da Silva y Cintia Corsini por su ayuda y amabilidad durante mi visita a esa ciudad a la que quiero regresar, Santa Teresa. Aquí quiero aprovechar para agradecer a Dayse Dias por la ayuda que me brindó durante mi viaje a Espírito Santo y por hacerme conocer al menos por unas horas la linda ciudad de Vitoria. A mi primer asesor, Víctor Pacheco, que siempre me recibe cordialmente en cada visita que hago a mi alma mater, el Museo de Historia Natural de Lima. De la misma forma agradezco a Pamela Sanchez y a todos los nuevos alumnos del laboratorio. A todos mis amigos esparcidos por Brasil y el mundo: Anderson Feijo por la ayuda en mis análisis y en la edición de imágenes; a Guillermo Cassini, Elis Damasceno y Thomas Püschel por el apoyo en mis análisis morfo-geométricos, mil disculpas por tantas incomodidades que les hice pasar; a mi buen amigo andino Sergio “marginal” Bolívar, por la ayuda en la parte estadística y todas las buenas conversaciones a la hora del almuerzo. A mi gran amiga Cindy Hurtado que, a pesar de la distancia, nuestra amistad perdura y no se convirtió en un impedimento para seguir trabajando juntos. Mil gracias por toda la ayuda brindada en la parte estadística durante el desarrollo de mi trabajo. Al Dr. Alfred Rosenberger por alentarme a realizar este proyecto, su ayuda y su amistad en los últimos años me han incentivado a ser un mejor científico y una mejor persona. Al Dr. Marcelo Tejedor, por el apoyo y la buena disposición que siempre me ha mostrado durante tanto tiempo. A los responsables de que este trabajo haya sido terminado, mis grandes amigos y co- orientadores “no oficiales”, Fabio Oliveira do Nascimento y Guilherme Siniciato Terra Garbino. Faltarían páginas para agradecerles por toda la ayuda brindada además de todas conversaciones científicas, los debates, los consejos, etc. Gracias por apoyarme siempre. A Fabiano R. de Melo por la ayuda desinteresada durante el desarrollo de este proyecto y la valiosa información compartida. También me gustaría agradecer a las siguientes personas por la gentil cesión de material fotográfico crucial para la evaluación de caracteres: Paula Breves, Carla Possamai, Dr. Adriano Chiarello, Daniel da Silva Ferraz, Theo Anderson, Luiz Dias y el Prof. Braz Cozenza. A Sergio Lucena por compartir conmigo información y bibliografía relevante para mi trabajo. A mi gran amiga Rafaela “xili” Vendramel, que además de ser mi colega (y traductora oficial), alegró mi estancia en São Paulo y en el laboratorio, gracias por las clases de Portugués Paranaense y por ayudarme en cada etapa de esta maestría. Quiero agradecerle también a mi amiga Yolanda “pirulito” Salgueiro por la ayuda en la redacción de mi trabajo, sin tu ayuda hubiera dormido muchas menos horas. A mis compañeros de casa Tulio, Michel y Diego “huachin” Evangelista, por los buenos y los malos momentos que pasamos durante nuestra convivencia. A ti Camila Cardoso por todo el amor, compresión y apoyo que me has brindado desde que nos conocimos y especialmente durante estos últimos meses de tanta presión. Mil gracias por quedarte siempre a mi lado. Por último, pero no menos importante, a mis padres mi gordita Elisa y mi viejo Juan, porque a pesar de no estar físicamente a mi lado nunca dejaron de apoyarme. A mi hermana Paola por todo tu apoyo. A mis abuelos Irene y Miguel, que desde mis primeros años me brindaron todo su ayuda y que, al igual que mis padres, se preocuparon por mi educación. Gracias a todos ustedes estoy aquí ahora. Estoy más que seguro que lamentablemente estoy dejando de mencionar a muchas personas que me ayudaron de una u otra manera durante el desarrollo de mi trabajo y a todas ellas les pido mi más sinceras disculpas. Este trabajo fue financiado por CAPES. Agradezco también a Idea Wild por la gentil donación de una cámara fotográfica profesional que fue de vital importancia para el desarrollo de mi proyecto. Abstract Muriquis, genus Brachyteles Spix, 1823, are the largest of the extant New World primates, and they are one of the three extant genera of the subfamily Atelinae along with Ateles (spider monkeys) and Lagothrix (wooly monkeys). The taxonomy of Brachyteles has constantly changed since its first description in the 19th century. First treated as a monotypic genus, and after several modifications in the number of species, Brachyteles currently contains two species, B. arachnoides (Southern muriqui) and B. hypoxanthus (Northern muriqui). The morphological evidence for this taxonomic arrangement relies on two diagnostic characters: the occurrence of a black-pigmented face and the absence of the first digit (thumb) in Southern muriqui populations vs. mottled face and fully-developed thumb in Northern muriqui populations. In addition, the phylogenetic relationship between atelines is disputed: on the one hand, the molecular evidence suggests an (Ateles (Brachyteles + Lagothrix)) clade and, on the other, most morphological evidence supports a clade (Lagothrix (Ateles + Brachyteles)) based on the high degree of postcranial and locomotory resemblances between Ateles and Brachyteles. My aims here are: 1) to verify how many taxa at the species level group there are in Brachyteles, and 2) to estimate the phylogenetic relationships among Atelinae using morphological characters. To achieve these goals, I have performed a qualitative analysis of external morphological characters as the presence or absence of the thumb, pelage coloration, and face pigmentation to test sexual dimorphism or dichromatism and intrapopulational variation. I also performed linear and geometric morphometrics analyses to test sexual dimorphism and geographical variation in both size and shape of the skull. Finally, I carried out a morphological phylogeny using 74 discrete morphological characters, two ecological and one karyological. This analysis includes 11 species of extant and fossil atelids and the outgroup was composed of Sapajus nigritus and Callicebus personatus. The analysis of the pelage coloration reveals that there is no sexual dimorphism or dichromatism in Brachyteles; besides, the pelage presents a high degree of individual variation.
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