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Diversification of Muroid Rodents Driven by the Late Miocene Global Cooling Nelish Pradhan University of Vermont

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Diversification of Muroid Rodents Driven by the Late Miocene Global Cooling Nelish Pradhan University of Vermont University of Vermont ScholarWorks @ UVM Graduate College Dissertations and Theses Dissertations and Theses 2018 Diversification Of Muroid Rodents Driven By The Late Miocene Global Cooling Nelish Pradhan University of Vermont Follow this and additional works at: https://scholarworks.uvm.edu/graddis Part of the Biochemistry, Biophysics, and Structural Biology Commons, Evolution Commons, and the Zoology Commons Recommended Citation Pradhan, Nelish, "Diversification Of Muroid Rodents Driven By The Late Miocene Global Cooling" (2018). Graduate College Dissertations and Theses. 907. https://scholarworks.uvm.edu/graddis/907 This Dissertation is brought to you for free and open access by the Dissertations and Theses at ScholarWorks @ UVM. It has been accepted for inclusion in Graduate College Dissertations and Theses by an authorized administrator of ScholarWorks @ UVM. For more information, please contact [email protected]. DIVERSIFICATION OF MUROID RODENTS DRIVEN BY THE LATE MIOCENE GLOBAL COOLING A Dissertation Presented by Nelish Pradhan to The Faculty of the Graduate College of The University of Vermont In Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy Specializing in Biology May, 2018 Defense Date: January 8, 2018 Dissertation Examination Committee: C. William Kilpatrick, Ph.D., Advisor David S. Barrington, Ph.D., Chairperson Ingi Agnarsson, Ph.D. Lori Stevens, Ph.D. Sara I. Helms Cahan, Ph.D. Cynthia J. Forehand, Ph.D., Dean of the Graduate College ABSTRACT Late Miocene, 8 to 6 million years ago (Ma), climatic changes brought about dramatic floral and faunal changes. Cooler and drier climates that prevailed in the Late Miocene led to expansion of grasslands and retreat of forests at a global scale. Palaeogeographic studies suggest a global vegetation change causing an abrupt increase in C4 plant biomass while C3 biomass decreased between 8 and 6 Ma. Subsequent cycles of cooler and drier climatic conditions during the Mid-Pliocene (3.5–3 Ma) and Pleistocene (2.8–2.5; 1.8–1.6; 1.0–0.8 Ma) also caused forests to retreat into isolated refugia which played an important role in events that led speciation and radiation of Muroid (Order Rodentia, Superfamily Muroidea) rodents. Muroid rodents are comprised of 6 families (Placanthomyidae, Spalacidae, Calomyscidae, Nesomyidae, Cricetidae, and Muridae) and make up close to one-third of named mammal species. Family Cricetidae and Muridae are especially speciose (containing ~1600 species altogether) and much of the diversity within these families arose during or after the Late Miocene. My dissertation deals with the systematics and historical biogeography of these fast-evolving groups of rodents with an emphasis on the genera Apodemus and Hybomys (Subfamily Murinae, Family Muridae), and Neodon (Subfamily Arvicolinae, Family Cricetidae). Habitat specialists such as Apodemus that occupy broadleaf forests, and Hybomys that occupy rainforests were likely isolated in forest refugia after the retreat of forests facilitating allopatric speciation. While voles in the subfamily Arvicolinae, that are associated with grasslands, expanded their range when forests retreated and speciated when grasslands retreated. In addition, field work carried out for this project in Nepal included several localities previously not sampled for small mammals. Most of Nepal is poorly surveyed and the first chapter focuses on the history of mammalogical surveys in Nepal and adds new localities for small mammal species, expanding the known range of the Nepalese endemic Himalayan wood mouse (Apodemus gurkha). ACKNOWLEDGEMENTS I am sincerely grateful towards my adviser, Bill Kilpatrick, for the opportunity to work on this project and encouraging me to tackle tangential projects which turned out to be a substantial part of my dissertation. I am thankful for the advice, continual support, and invaluable experience provided by Bill. Bill has always been extremely generous with his time, knowledge, and funds. I am equally thankful to Bill for allowing me independence to learn on my own and for the opportunity to work in Nepal. I am a better scientist because of him and I have Bill to thank for making my Ph.D. a highly enlightening and enjoyable process. I thank my committee members (Dave Barrington, Ingi Agnrasson, Lori Stevens, Sara Helms Cahan) for their support, knowledge, and feedback. Thank you, Dave, for your infectious enthusiasm and insights on details that would have otherwise escaped me. Thank you, Ingi, for your knowledge and honest advice on work and life. Thank you, Lori, for your knowledge and I have learned a lot from the kindness you show to others. Thank you, Sara, for your questions and advice which not only made my work better but also made me a better teacher. I am also grateful to my field team in Nepal. Without the help of Saurav, Maila, Krishna, Pemba, Ganga, Sajan, Paski, and Ramesh, I would not have any samples to work with. I am also grateful to the staff at the Center for Molecular Dynamics Nepal especially Ajay Narayan Sharma, Adarsh Man Sherchan, Jyoti Joshi, and Priya Joshi. Sequencing specimens from Nepal was only possible with their help. Special thank you to my mom, Lily Pradhan, who procured permits to carryout sampling in Nepal. ii I also extend my thanks towards past members of the Kilpatrick lab, Ryan Norris, Jan Decher, and Chris Gray. Chapter 4 without their help and without the help of co-author Mike Carleton would not have been possible. Ryan has also been free with his advice for which I am thankful. Thanks to the undergraduate interns who made lab work possible. They are Cody Aylward, Rachel Rollins, Cassidy Francik, Devon Farr, Ben Torpey, and Adriana Jurich. Field work in Nepal was supported by the Grants in Aid from the American Society of Mammalogists and the Carolyn M. Glass Fund. Laboratory work was funded by Graduate Research support from the University of Vermont, NSF, NSF EPSCoR, and USFWS International Division to Bill Kilpatrick and an Ohio State College of Arts and Sciences Regional Campus Faculty Research/Creative Activity grant and by startup funds to Ryan Norris. I also thank Dr. Bruce Patterson and John Phelps from the Field Museum, Darrin Lunde and Nicole Edmison from the Smithsonian National Museum of Natural History, and Dr. Violaine Nicolas from the Muséum national d'Histoire naturelle for loaning and providing access to the specimens in the research collection. Thank you is extended to various agencies for funding and collection permits. Lastly, I would like to thank my parents (Lily Pradhan and Netra Lal Pradhan), my uncle, aunt and cousins (Vickram Chhetri, Yvonne Chhetri, Abhishek and Saurav), and my extended family for their love, belief and support. Finally, I extend my love and gratitude to my beloved wife, Paliza Shrestha, for her unconditional love, support, and belief which got me through my Ph.D. I am in great debt to everyone without whose help, I would not have achieved anything. iii TABLE OF CONTENTS ACKNOWLEDGEMENTS ................................................................................................ ii LIST OF TABLES ............................................................................................................ vii LIST OF FIGURES .............................................................................................................x CHAPTER 1: New records of small mammals from Central Nepal ...................................1 1.1 Abstract ..................................................................................................................... 1 1.2 History of small mammal surveys in Nepal .............................................................. 1 1.3 Trapping Locality Descriptions ................................................................................. 4 1.3.1 Annapurna Conservation Area (ACA) ............................................................... 4 1.3.2 Manaslu Conservation Area (MCA)................................................................... 4 1.3.3 Shey Phoksundo National Park (SPNP) ............................................................. 5 1.3 New Records of Small Mammals ............................................................................. 6 1.5 Literature Cited ......................................................................................................... 7 CHAPTER 2: Phylogenetic relationships and biogeography of Apodemus (Muridae: Murinae: Apodemini).........................................................................................................13 2.1 Abstract ................................................................................................................... 13 2.2 Introduction ............................................................................................................. 14 2.3 Materials and Methods ............................................................................................ 18 2.3.1 Specimens and taxonomic sampling................................................................. 18 2.3.2 DNA extraction, sequencing, and alignment .................................................... 20 2.3.3 Genetic distance, phylogenetic analyses, and divergence times ...................... 22 2.4 Results ..................................................................................................................... 24 2.5 Discussion ............................................................................................................... 26 2.5.1 Tribal
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