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Phylogeography of Southeast Asian Flying Foxes (Chiroptera: Pteropodidae: Pteropus)

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Phylogeography of Southeast Asian Flying Foxes (Chiroptera: Pteropodidae: Pteropus) City University of New York (CUNY) CUNY Academic Works All Dissertations, Theses, and Capstone Projects Dissertations, Theses, and Capstone Projects 5-2015 Phylogeography of Southeast Asian flying foxes (Chiroptera: Pteropodidae: Pteropus) Susan Man Shu Tsang 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/1161 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] Phylogeography of Southeast Asian flying foxes (Chiroptera: Pteropodidae: Pteropus) By Susan M. Tsang 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 2015 © 2015 Susan M. Tsang All Rights Reserved ii This manuscript has been read and accepted for the Graduate Faculty in Biology in satisfaction of the dissertation requirement for the degree of Doctor of Philosophy. ___________________ ______________________________________________ Date Chair of Examining Committee Dr. David J. Lohman, City College ___________________ ______________________________________________ Date Executive Officer Dr. Laurel A. Eckhardt ______________________________________________ Dr. Michael J. Hickerson, City College ______________________________________________ Dr. Nancy B. Simmons, American Museum of Natural History ______________________________________________ Dr. Kristofer M. Helgen, National Museum of Natural History, Smithsonian Institute ______________________________________________ Dr. Tigga Kingston, Texas Tech University ______________________________________________ Supervising Committee The City University of New York iii ABSTRACT Phylogeography of Southeast Asian flying foxes (Chiroptera: Pteropodidae: Pteropus) By Susan M. Tsang Advisor: David J. Lohman Flying foxes (Pteropus) are a genus of Old World fruit bats that are important seed dispersers and pollinators for plants native to the 200,000+ islands in Southeast Asia, yet they are some of the most poorly known bats in the world. They comprise some of the largest known bat species, and are morphologically relatively conserved on the genus level. Pteropus is the most species-rich genus within Pteropodidae, though the origin for this diversity remains incompletely understood. In Chapter 1, I discuss the importance of Pteropus to the ecosystem and as reservoir hosts. In Chapter 2, a molecular phylogeny is presented with Pteropus species organized into fewer species groups than recognized from previous research that better reflected the comprehensive dataset. An increase in relative divergence rate was detected within Pteropus during the Pliocene that led to rapid radiations in three species groups. Additionally, discordant signals from nuclear and mitochondrial genes suggested incomplete lineage sorting and hybridization were present, likely as a result of the young clade age, low genetic variability, and rapid diversification of the genus. In Chapter 3, using the species tree generated in Chapter 2, I tested biogeographic mechanisms and scenarios that resulted in current distributions of Pteropus species using several ancestral area reconstruction methods. Dispersal and founder-event speciation were both important mechanisms through which species expanded into new areas. Wallacea was an integral part of the evolutionary history of Pteropus, and likely the region of iv origin, a new result uncovered largely a product of the increased taxonomic and geographic sampling. I then used a combination of phylogenetics and population genetics to determine the population connectivity of two commonly studied Pteropus hosts that are of interest to the disease ecology community, P. vampyrus (Chapter 4) and P. alecto (Chapter 5). Host metapopulation dynamics are important for predictions of pathogen diversity, aggressiveness, and transmission. Pteropus vampyrus and P. alecto highlight differences in management strategies needed and pathogen model predictions. Chapter 6 presents a general discussion regarding these findings and future directions for research. v ACKNOWLEDGMENTS This dissertation would not have been possible without the support of many friends and colleagues. First, my thanks go to my committee for being willing to take a chance on this unknown and naïve student that kept pestering them: David Lohman for the late nights writing grants, all the good times in the field and in the lab, and making this entire process less daunting; Nancy Simmons for being as excited as I am for every single bat I get; Michael Hickerson for teaching and reminding me how much fun it is to get an analysis working all by myself; Tigga Kingston for bringing me into SEABCRU and introducing me to so many fantastic researchers throughout Southeast Asia; and Kristofer Helgen for understanding and sharing in my fascination with Maluku and giant fruit bats. I deeply appreciate all the advice you have all given me throughout the years. Your guidance has been vital to my growth and I look forward to continuing to learn from all of you. Financially, I have been supported by the Biology Department at the Graduate Center and City College of New York through the CUNY Science Scholarship, teaching assistantships, and travel grants. Thanks to the National Science Foundation for supporting me through the Science Now GK-12 Teaching Fellowship and the East Asia Pacific Summer Institute Fellowship in Singapore (OISE-1108298), and for travel funds from the RCN grant for the Southeast Asian Bat Conservation Research Unit (DEB 1051363, PI: Tigga Kingston). For the final years of my dissertation and related fieldwork expenses, I thank the National Institute of Health for financing our bat-borne pathogen study (1R21AI105050, PI: David J. Lohman). I also owe a great deal to the Fulbright Program, the American Indonesian Exchange Foundation, and the Department of State for financial and logistical support during my year abroad in Indonesia. And a special thanks to the generous fuelers who supported my project through the first #SciFund vi crowdfunding initiative on RocketHub—without their donations, the first steps of this project would not have been possible. Additional funding for fieldwork and lab work was provided by the American Philosophical Society through the Lewis and Clark Exploration Fund and the National Geographic Society Committee for Research and Exploration through the Young Explorers Grant (9272-13). Conference support was also provided by the Southeast Asian Gateway Evolution research group. I am greatly indebted to George Barrowclough and Joel Cracraft for allowing me to use their molecular lab in the Department of Ornithology at AMNH for the past few years. My thanks to everyone in the ornithology department, especially Jeff Groth and Jonas Lai, for their guidance and good humor when nothing seems to go right in the lab. Molecular work in the Monell and Cullman lab is supported by the Dorothy Cullman Foundation. Additional thanks to everyone in the Department of Mammalogy and Research Library for helping me with specimen access, accounting, permits, general bureaucracy, and requests for really obscure taxonomic literature. As this was a multinational undertaking, there are countless people to thank in each country, in particular: Sigit Wiantoro, my Indonesian brother, for being patient, looking out for me, and making sure we always get a bat; Maria Josefa “Sweepea” Veluz, for being willing to take buses throughout the Philippines for six hours just to get permission to conduct fieldwork; Ian Mendenhall, for starting me on this disease-ridden adventure; members of the EvoLab at the National University of Singapore for giving me a floor to sleep on whenever I needed to swing by for meetings, embarrassing stories of Dave, and overnight MahJong; my students from all over the world, who have helped a great deal with resolving bureaucratic matters and contributed to the completion of this project’s labwork and continued conservation efforts; and past and vii present members of the Lohman Lab at CCNY, for tea at 3 PM, lobsters in Chelsea, and margaritas at Picante. I am exceedingly grateful for all my friends and colleagues at CUNY and AMNH for believing in my success even when I did not, especially my cohort-mates and all the members of the Hickerson Lab. I am excited for the plans we have made to continue working together as we continue to grow after this first step. There are so many people who I have met at meetings and countless others who have provided me with invaluable information on field sites that there is not enough space to list them all, but I am profoundly grateful for your contributions to my research. This project would not have been possible without the incredible level of hospitality I have experienced everywhere I have been, both domestically and internationally. To my friends at both MZB-LIPI and NMP, I will be seeing you all shortly and we will celebrate in person. Specimen collection would not have been possible without the permissions granted by the Ministry of Foreign Research and Ministry of Forestry in Indonesia, the Department of Environment and Natural Resources in the Philippines, the Ministry of the Environment, Forests, and Tourism and Madagascar National Parks in Madagascar, and local government entities. I thank the forestry personnel and guides for their
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