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Systematics of the American Marsupial Genus Marmosops (Didelphidae: Thylamyini) Based on Molecular and Morphological Data

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Systematics of the American Marsupial Genus Marmosops (Didelphidae: Thylamyini) Based on Molecular and Morphological Data Systematics of the American marsupial genus Marmosops (Didelphidae: Thylamyini) based on molecular and morphological data A DISSERTATION SUBMITTED TO THE FACULTY OF UNIVERSITY OF MINNESOTA BY Juan Fernando Díaz Nieto IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Sharon A. Jansa April 2016 © Juan Fernando Díaz Nieto 2016 ACKNOWLEDGEMENTS This dissertation is the product of contributions from many people over the course of several years, but above all I want to thank my advisor, Sharon A. Jansa for her extreme patience and constant support during all the years I spent in Minnesota and my final years in Colombia. From the first day to the last, Sharon constantly gave me lessons not only about systematics, lab work, English writing, or mammals, but also, with her own day-to-day example, she showed me the value of critical thinking and rigor in the life of a scientist. Without any doubt Sharon will always be an example to follow, thank you Sharon. Another person who merits all my gratitude is Robert S. Voss, who has been more than a vital collaborator in this research (he made significant contributions to all three chapters of this dissertation). Rob has also been a great teacher during my years as a graduate student. From Rob I learned more than just mammalian systematics, probably his most important lessons were: to pay attention to detail, to work hard, and to think before speaking. I feel truly honored to have learned from one of the greatest mammalian systematists. My committee members, Keith Barker, Scott Lanyon, and Andrew Simons were crucial for developing a clear path in what can initially be the obscure road of the dissertation. They were especially helpful in providing advice and asking the right questions that would help me focus my research. Discussion on early stages of my i dissertation chapters were kindly provided by Keith Barker, Lorissa Fujishin, Tom Giarla, and Danielle Drabeck. I am grateful to the many curators and collection support staff that hosted my visits and processed the loans that made this study possible, especially (in no particular order) Alejandra Camacho and Santiago Burneo (QCAZ); Ana Carmignotto (MZUSP); Bruce Patterson and the late Bill Stanley (FMNH); Burton K. Lim and Jacquiline Miller (ROM); Francisco Bisbal-E. and Javier Sánchez-H. (EBRG); Hugo López-Arévalo, Catalina Cárdenas, and Miguel E. Rodríguez-Posada (ICN); James L. Patton, Eileen Lacey, and Chris Conroy (MVZ); John R. Wible and Susan B. McLaren (CM); Joseph Cook and Jonathan Dunnum (MSB); Julián A. Salazar and Juan D. Corrales-Escobar (MHNUC); Kristofer M. Helgen, Linda K. Gordon, and Darrin P. Lunde (USNM); Luis Albuja V. (EPN); Paula Jenkins (BMNH); Phil Myers (UMMZ); Sergio Solari and Juan M. Martínez-C. (CTUA); Teresa Tarifa (CBF); Victor Pacheco (MUSM); Mark Hafner (LSUMZ); Jim Dines ( LACM); François Catzeflis (ISEM); Louise Emmons (for material that will eventually be deposited at MNK), Fernando Quintela (for material that will eventually be deposited at FURB); and Guillermo D’Elía (for material that will eventually be deposited at MNHNP). Diego Alvarado-Serrano, Paul Velazco, and Robert P. Anderson provided DNA and tissue samples collected by each of them in independent fieldwork in Ecuador, Peru, and Venezuela, respectively. I am particularly grateful to James L. Patton for unselfishly sharing with me CYTB sequences from many taxa that helped me to increase the taxon and geographic sampling used in this work. All the laboratory work could not have been accomplished ii without the help of Tom Giarla, Lorissa Fujishin, and Carmen Martin. I would also want to thank Patricia J. Wynne (illustrator-in-residence in the AMNH Department of Mammalogy) for her splendid line art, and Suzann Goldberg (in the AMNH Department of Paleontology) for her excellent cranial photographs, both of their contributions can be appreciated in Chapter 2. This work was funded in part by National Science Foundation research grants DEB-743062 (to Sharon A. Jansa), DEB-743039 (to Robert S. Voss) and by a Doctoral Dissertation Improvement Grant DDIG-1311163 (to Sharon A. Jansa and me). I would also like to acknowledge a Grant-in-Aid of Research from the American Society of Mammalogists and a James W. Wilkie Fund for Natural History Fellowship from the J.F. Bell Museum of Natural History (University of Minnesota), both of which provided additional funding to visit museum collections. I am currently supported by a Francisco José de Caldas Fellowship from the Colombian department of science, technology, and innovation (COLCIENCIAS). My friends in the Twin Cities contributed to my happiness throughout my studies: Maga, Alejo, Cesitar, Jose, María (un abrazo para todos). Tom, Mike, and Danielle generated the best possible working environment in our office, they always had time for a good laugh. Sharon, Keith, Sean, and Alex always welcomed me (and Caro) as members of their home, I will always be grateful for that. Lastly, I want to thank my wife Carito for her unconditional company through many winters in Minnesota, she always gave joy to my life. iii DEDICATION This thesis is dedicated to my mom, Carito and Titi, three women from whom I have received the most important "lectures" of my life. iv ABSTRACT This research presents the results of a collaborative work with Sharon A. Jansa and Robert S. Voss on the taxonomy and systematics of the American marsupials of the genus Marmosops and some of its closely allied forms. Chapter 1 evaluates the species- level diversity of the genus Marmosops using mitochondrial sequences from >200 specimens, including exemplars of every currently recognized species together with a dense intraspecific sampling. These data are analyzed using the General Mixed Yule Coalescent (GMYC) model and the results suggest that the genus could be twice as speciose as currently recognized. Additionally, the phylogenetic relationships within Marmosops are evaluated using sequences of the Breast Cancer Type 1 susceptibility gene (BRCA1). These analyses reveal a basal dichotomy between two ancient, morphologically diagnosable clades. Based on the latter results, a taxonomic proposal is made with the description of a new subgenus, Sciophanes. Chapter 2 includes a revision of the species of subgenus Sciophanes in the context of the molecular analyses of Chapter 1. This revision recognizes 12 valid species in three monophyletic species groups: the Parvidens Group (including M. pakaraimae, M. parvidens, and M. pinheiroi), the Fuscatus Group (M. carri, M. fuscatus, M. handleyi, and M. invictus), and the Bishopi Group (M. bishopi, M. juninensis, M. ojastii, and two new species). For each species, information about type material, ecogeographic distribution, and diagnostic morphological characters is presented. Chapter 3 evaluates the phylogenetic relationships of the tribe Thylamyini (a clade that includes the genus Marmosops) by v using a multi-locus dataset. In particular, this chapter aims to resolve evolutionary relationships of the thylamyine genus Chacodelphys, a monotypic genus that has remained a phylogenetic enigma since its original description in 1930. A previous understanding of the species-level diversity within Marmosops is crucial for constructing a phylogeny of Thyamyini because this genus accounts for almost 45% of the diversity within the tribe. Phylogenetic analyses of these data convincingly resolves Chacodelphys as the sister taxon of Cryptonanus, a genus with which it had not previously been thought to be closely related, and supports most of the previous phylogenetic arrangements obtained within Marmosops. vi TABLE OF CONTENTS LIST OF TABLES ............................................................................................................ x LIST OF FIGURES ......................................................................................................... xi CHAPTER 1. DNA SEQUENCING REVEALS UNEXPECTED RECENT DIVERSITY AND AN ANCIENT DICHOTOMY IN THE AMERICAN MARSUPIAL GENUS MARMOSOPS (DIDELPHIDAE: THYLAMYINI) .............. 1 INTRODUCTION ........................................................................................................ 1 METHODS .................................................................................................................... 4 Taxon Sampling and specimen identification ............................................................. 4 Laboratory methods and sequence alignment ............................................................. 5 Putative species delimitation based on CYTB sequences ......................................... 15 Phylogenetic analyses of BRCA1 and BRCA1 + CYTB ......................................... 18 RESULTS .................................................................................................................... 19 Phylogenetic analyses and species delimitation based on CYTB sequence data ..... 19 Phylogenetic relationships ........................................................................................ 23 DISCUSSION .............................................................................................................. 27 Assessment of species-level diversity and phylogenetics in Marmosops ................. 27 Taxonomic accounts ................................................................................................. 30 Sciophanes, new subgenus ........................................................................................ 30 Subgenus Marmosops Matschie, 1916 ....................................................................
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