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Systematics, Biogeography, and Phylogeography of Thylamys Mouse Opossums, a Recent Radiation of Neotropical Marsupials

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Systematics, Biogeography, and Phylogeography of Thylamys Mouse Opossums, a Recent Radiation of Neotropical Marsupials Systematics, Biogeography, and Phylogeography of Thylamys Mouse Opossums, a Recent Radiation of Neotropical Marsupials A DISSERTATION SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL OF THE UNIVERSITY OF MINNESOTA BY Thomas Christopher Giarla IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Sharon A. Jansa August 2013 © Thomas Christopher Giarla 2013 ACKNOWLEDGEMENTS This dissertation would have been impossible without the kindness, support, and advice of my advisor, Sharon Jansa, who pushed me to follow my independent interests and provided me with the resources and connections that have led to its successful completion. Robert Voss was a crucial collaborator, especially as I was first developing my project. His eye for detail improved this project immeasurably, and he contributed substantially to Chapters 1 and 2. Discussions with my committee members, Keith Barker, Ken Kozak, and Andrew Simons, enriched my understanding of important methodological issues and helped narrow my research questions. Discussions and comments on earlier drafts of each chapter were generously provided by Andrew Simons, Keith Barker, Robert Voss, Juan Diaz, Silvia Pavan, and Robert Anderson. This work was supported by two grants from the National Science Foundation: DEB-1110365 to Sharon Jansa and me and DEB-0743062 to Sharon Jansa and Robert Voss. Additional funds were provided by the University of Minnesota, the Bell Museum of Natural History, the American Society of Mammalogists, and the Society of Systematic Biologists. Molecular work for this project was completed with help from Tracy Smelter, Tim Sosa, Courtney Comar, and Lorissa Fujishin. Museum curators, curatorial assistants, and collectors from all over the world generously provided tissues and morphological specimens. During fieldwork in Argentina, Gabriel Martin was my colleague, guide, and translator, and for that I am grateful. I would like to acknowledge the amazing, encouraging team of mentors, colleagues, and friends that I have met at the i University of Minnesota. Without them, this whole endeavor would have been much less fun and enriching. I also want to thank my dear friend Rafael Walker, who encouraged me to pursue a Ph.D. in the first place and supported me from start to finish. Finally, I thank my husband, Dan Covich, who moved half-way across the country and altered his career plans to be with me in Minnesota. He helped me escape the academic bubble every now and then, keeping me sane, healthy, and happy over the past six years. ii DEDICATION I dedicate this dissertation to my parents, who fostered my love for biology by filling my childhood with bug collections, exotic vacations, odd pets, and a backyard biome worth exploring. iii ABSTRACT This project broadly explores the systematics, biogeography, and phylogeography of Thylamys mouse opossums, a genus of Neotropical marsupials from central and southern South America. Chapter 1 is part of a collaborative work with Robert Voss and Sharon Jansa. In it, we resolve longstanding issues surrounding Thylamys taxonomy and nomenclature using mitochondrial DNA sequences and morphology, and provide the first phylogenetic hypothesis for all recognized species in this genus. We recognize nine species but also uncover numerous morphologically cryptic mitochondrial haplogroups within four species. In Chapter 2, I assess the evolutionary independence of a subset of these morphologically cryptic lineages within the montane species T. pallidior, T. sponsorius, and T. venustus. I find evidence to support the existence of two lineages within each of the three species, and also conduct tests to determine the number of nuclear loci needed to confidently test species limits. In Chapter 3, I examine the biogeographic history of Thylamys and its monotypic sister-genus Lestodelphys, considering the impact of habitat type and physical barriers on range evolution and cladogenesis. In Chapter 4, I test predictions regarding the impact of late Quaternary glacial cycles on the evolutionary history of six montane cryptic lineages. I estimate divergence times and demographic shifts for each lineage, and find limited support for the core predictions. Two supplementary files are provided online as part of this dissertation: a file containing 15 phylogenetic trees for each of the loci considered in Chapter 2 (Online Supplementary File 1) and a file containing GenBank accession iv numbers and tissue voucher numbers for the sequences included in the supermatrix in Chapter 3 (Online Supplementary File 2). v TABLE OF CONTENTS List Of Tables ................................................................................................................. viii List Of Figures .................................................................................................................. ix Chapter 1, Species Limits and Phylogenetic Relationships in the Didelphid Marsupial Genus Thylamys Based on Mitochondrial DNA Sequences and Morphology ..........................................................................1 INTRODUCTION ..................................................................................................................... 1 Taxonomic History .................................................................................................................. 2 Species Recognition Criteria ................................................................................................... 3 MATERIALS AND METHODS .............................................................................................. 5 Museum Collections ................................................................................................................ 5 Taxon Sampling ...................................................................................................................... 6 DNA Extraction and Gene Sequencing ................................................................................... 7 Phylogenetic Analyses ............................................................................................................ 8 Morphology ........................................................................................................................... 12 RESULTS ................................................................................................................................. 13 Sequence Characteristics ....................................................................................................... 13 Phylogenetic Analyses .......................................................................................................... 15 DISCUSSION ........................................................................................................................... 31 Chapter 2, Hidden Diversity in the Andes: Comparison of Species Delimitation Methods in Montane Marsupials .........................................35 INTRODUCTION ................................................................................................................... 35 MATERIALS AND METHODS ............................................................................................ 38 Nuclear Marker Design ......................................................................................................... 38 Sampling of Loci and Individuals ......................................................................................... 41 Haplotype Phasing, Sequence Alignment, and Neutrality Tests ........................................... 43 Gene Trees and “Species” Trees ........................................................................................... 44 Bayesian “Species” Delimitation in BPP Using Ndna .......................................................... 45 Species Delimitation in Spedestem ....................................................................................... 52 RESULTS ................................................................................................................................. 53 Gene Tree and Species Tree Results ..................................................................................... 53 Species Delimitation Using BPP With Fifteen Nuclear Loci ................................................ 56 Species Limit Validation Using Spedestem .......................................................................... 59 DISCUSSION ........................................................................................................................... 61 Comparison of “Species Delimitation” Methods .................................................................. 61 Lineage Recognition Using Mitochondrial vs. Nuclear Loci ................................................ 65 A Large Number of Loci Might Not Be Needed to Identify Cryptic Lineages .................... 67 vi Introgression Detected Between Two Species ...................................................................... 69 Are These Cryptic Lineages Species? ................................................................................... 71 Chapter 3, The Role of Physical Geography and Habitat Type in the Biogeographic History of an Ecologically Varied and Recent Radiation of Neotropical Mammals ............................................................................74 INTRODUCTION ................................................................................................................... 74 MATERIALS AND METHODS ...........................................................................................
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