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Didelphidae: Monodelphis) City University of New York (CUNY) CUNY Academic Works All Dissertations, Theses, and Capstone Projects Dissertations, Theses, and Capstone Projects 9-2016 Phylogeny, Systematics and Biogeography of Short-Tailed Opossums (Didelphidae: Monodelphis) Silvia E. Pavan The Graduate Center, City University of New York How does access to this work benefit ou?y Let us know! More information about this work at: https://academicworks.cuny.edu/gc_etds/1472 Discover additional works at: https://academicworks.cuny.edu This work is made publicly available by the City University of New York (CUNY). Contact: [email protected] PHYLOGENY, SYSTEMATICS AND BIOGEOGRAPHY OF SHORT-TAILED OPOSSUMS (DIDELPHIDAE: MONODELPHIS) by SILVIA ELIZA D’OLIVEIRA PAVAN A dissertation submitted to the Graduate Faculty in Biology in partial fulfillment of the requirements for the degree of Doctor of Philosophy, The City University of New York 2016 © 2016 SILVIA ELIZA D’OLIVEIRA PAVAN All Rights Reserved ii This manuscript has been read and accepted for the Graduate Faculty in Biology to satisfy the dissertation requirement for the degree of Doctor of Philosophy. _____________ ________________________________________________ Date Dr. Robert S. Voss, Chair of Examining Committee _____________ ________________________________________________ Date Dr. Laurel Ann Eckhardt, Executive Officer ______________________________________________________ Dr. Ana C. Carnaval ______________________________________________________ Dr. Nancy Simmons ______________________________________________________ Dr. Frank Burbrink ______________________________________________________ Dr. Sharon A. Jansa Supervisory Committee THE CITY UNIVERSITY OF NEW YORK iii Abstract Phylogeny, Systematics and Biogeography of short-tailed opossums (Didelphidae: Monodelphis) by Silvia Eliza D’Oliveira Pavan Advisor: Robert S. Voss Short-tailed opossums (genus Monodelphis) comprise the most species-rich genus of New World marsupials, with 25 currently recognized species. Monodelphis comprise small, terrestrial species collectively widespread in South America, which makes the group potentially informative about biogeographic processes that have shaped the continental fauna. The genus exhibits striking variation in several phenotypic characters, notably pelage coloration, behavior, and reproductive strategies. This diversity is unique among Neotropical marsupials, and makes the group particularly interesting to investigate the evolution and the adaptive significance of phenotypic trait variation. Despite this potential, missing knowledge on phylogeny and basic taxonomy precludes broader studies on evolution and biogeography on this group. To remedy this situation this thesis is centered on undertaking a comprehensive phylogenetic analysis and taxonomic revision of Monodelphis. In chapter one (published in collaboration with Dr. Sharon A. Jansa and Dr. Robert S. Voss) we present the first phylogenetic analyses of Monodelphis based on dense taxonomic sampling—23 of the 25 currently recognized species—and multiple genes—one mitochondrial gene (CYTB), two autosomal exons (IRBP, BRCA1), one autosomal intron (SLC38), and one X- iv linked intron (OGT). Parsimony, maximum-likelihood and Bayesian analyses of this dataset (110 terminals, 4983 aligned sites) strongly support the monophyly of Monodelphis and recover six major clades within the genus. Additionally, the analyses suggest that several nominal taxa are synonyms of other species in the genus (M. “sorex” of M. dimidiata, M. “theresa” of M. scalops, M. “rubida” and M. “umbristriata” of M. americana, and M. “maraxina” of M. glirina). By contrast, four unnamed genetic lineages recovered by the analyses may represent new species. Reconstructions of ancestral states of two discrete characters—dorsal pelage color pattern and habitat—suggest that the most recent common ancestor of Monodelphis was uniformly colored (with unpatterned dorsal pelage) and inhabited moist forest. Whereas most dorsal pelage patterns (e.g., reddish sides and reddish head-and-rump) appear to have evolved homoplastically in Monodelphis, dorsal stripes may have had a unique historical origin in this genus. In chapter two (also published in collaboration with Dr. Sharon A. Jansa and Dr. Robert S. Voss) we infer historical-biogeographic patterns and processes in South America based on estimated divergence times and ancestral distributions for this diverse clade of marsupials. The dating analysis suggests that the diversification of Monodelphis was not restricted to a narrow time interval, such that speciation cannot be attributed to a single causal historical factor. In particular, speciation within the Atlantic Forest biome appears to have occurred in the Neogene, whereas most Amazonian speciation events are Pleistocenic. Amazonia and the Atlantic Forest hosted most of the diversification events in Monodelphis and were estimated as the historical sources of lineages that subsequently colonized other areas (e.g., Tepuis, Andes, Cerrado) during the Pliocene and Pleistocene. Model selection suggests an important role for founder-event speciation, a process seldom accounted for in previous biogeographic analyses of continental v clades. These results, together with others recently reported from analyses of South American datasets suggest that dispersal-mediated cladogenesis has been an important process in the evolution of Neotropical vertebrate faunas. Possible mechanisms for founder-event speciation in low-vagility terrestrial vertebrates such as Monodelphis include historically transient connections between currently disjunct biomes and rapid reproductive isolation of populations colonizing adjacent but ecologically disparate biomes. In the following chapter (to be published in collaboration with Dr. Robert S. Voss), an integrative approachphylogenetic information together with phenotypic data from external and craniodental morphology is used to provide a revised subgeneric classification of Monodelphis, intended to serve as the basis for future revisionary research at the species level. Over 2000 specimens of Monodelphis were analyzed for morphology, including representative material of all species currently recognized as valid, together with all undescribed forms discussed in the previous chapters. Discrete characters found to be useful for diagnosing monophyletic groups of species previously established by molecular research are defined and illustrated. Five subgenera are formally recognized, for which morphological diagnosis, comparisons, and patterns of geographical distribution and sympatry are provided. In chapter four, a paper (already published) describing a new species of Monodelphis from Atlantic Forest in Brazil is presented. vi Acknowledgments I would like to thank my advisor, Rob Voss, for his guidance throughout these almost five years of work. Thank you for receiving me as your student, for sharing your knowledge and inspiring me to become more focused and objective in my research. Special thanks to Sharon Jansa, for her dedication and insightful participation during all phases of my dissertation, especially for her advise on the molecular work and phylogenetic methods. Also, I wish to express my deepest gratitude to my committee members Carol Carnaval, Frank Burbrink, Nancy Simmons and Paul Velazco for their support, constructive questioning and suggestions regarding this dissertation. Throughout my PhD I have received financial support from several institutions, including fellowships from the City University of New York and the American Museum of Natural History, and grants from Universidade de São Paulo, Labex CEBA (Centre d’étude de la biodiversité amazonienne), Smithsonian Institution (National Museum of Natural History), the Graduate Center in CUNY, and the American Society of Mammalogists (2015 Albert R. and Alma Shadle Fellowship). Many colleagues, curators, and collection support staff received me and helped during my visits to museums, permitted analysis of specimens under their care, loaned specimens, provided tissue samples, or assisted in other material ways. I am very greatfull to all of them, which are individualy listed on the acknowledge section of individual chapters. I could not fail to express my special gratitude to the mammalogy, ornithology, and RGGS staff at the American Museum of Natural History, which assisted me in several ways throughout my PhD: Aja Marcato, Anna Manuel, Beth Kneller, Catherine Doyle-Capitman, Eileen Westwig, Eleanor vii Hoeger, Elizabeth Sweeny, Jeff Groth, Jessica Shearer, Joel Cracraft, John Flynn, Jonas Lai, Maria Rios, Mary Knight, Neil Duncan, Nicole Edmison, Patricia Wynne, and William Mauck. Several friends kindly received me in their homes during my visits to scientific collections. Without their hospitality and company, my “field time” would have been certainly more arduous and less pleasant. Many thanks to Claudia Costa, Leonardo Vieira, Julia Calhau, Mônica Ulysséa, Vitor Piacentini, Luciano Moreira-Lima, Carla Quijada, Fernanda Santos, Marcelo Sturaro, Marcela Lima, Marcos Persio, Eliécer Gutierrez, José Padial, Jorge Cherém, Fernanda Cherém, Eduardo Cherem, and Laura Chornogubsky. I am very grateful to Lorissa Fujishin and Carmen Martin for help with molecular procedures and gene sequencing, to Willian Mauk and Juan Dias for assistance with initial sequence editing and phylogenetic analyses, and to Nick Matzke for help with ancestral range analyses. Many thanks to Adriano Maciel, Andrea Mesquita, Dante Pavan, Mario
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