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ASOCIAL MONOGAMY, EXTRA-PAIR PATERNITY, and DISPERSAL in the LARGE TREESHREW (Tupaia Tana)

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ASOCIAL MONOGAMY, EXTRA-PAIR PATERNITY, and DISPERSAL in the LARGE TREESHREW (Tupaia Tana) ABSTRACT Title of Document: ASOCIAL MONOGAMY, EXTRA-PAIR PATERNITY, AND DISPERSAL IN THE LARGE TREESHREW (Tupaia tana) Jason Munshi-South, Doctor of Philosophy, 2006 Directed By: Dr. Devra G. Kleiman, Adjunct Professor Behavior, Ecology, Evolution & Systematics Dr. Gerald S. Wilkinson, Professor Behavior, Ecology, Evolution & Systematics Monogamy occurs in only 5% of mammalian species, but is significantly more common in the Euarchonta: primates, dermopterans, and treeshrews (15% spp.). However, many of these species do not breed monogamously, indicating the need to understand behavioral and genetic monogamy as separate evolutionary phenomena. I examined monogamy in the large treeshrew (Tupaia tana) in Sabah, Malaysia using radiotelemetry data from 46 individuals tracked during and after a fruit masting episode in 1990-1991, during a non-masting period from 2002-2004, and in a selectively logged forest from 2003-2004. I show that large treeshrews exhibit behavioral monogamy in all these ecological situations. However, behavioral monogamy is best characterized as dispersed pair-living, or “asocial monogamy”, in this species because male-female pairs travel, forage, and sleep alone on their joint territories. Next, I use microsatellites and mitochondrial DNA d-loop haplotypes to analyze the genetic maternity and paternity of 24 T. tana offspring. I show one of the highest rates of extra-pair paternity (EPP) ever recorded for a behaviorally monogamous mammal. Over 40% of young were sired by males that were not the behavioral partner of their mother, and three litters exhibited evidence of multiple paternity. Comparative analysis of relative testis size in treeshrews and primates indicates that sperm competition is not associated with the high rates of EPP in T. tana, and that the evolution of monogamy is associated with the evolution of smaller testes. Finally, I find genetic evidence of female-biased dispersal and gene flow in large treeshrews. The vast majority of mammals exhibit the behavioral combination of polygyny and male-biased dispersal, but female-biased dispersal may evolve in monogamous species when females compete for ecological resources. In support of the local resource competition hypothesis, I find lower population assignment probabilities and pairwise relatedness for females than males. These results indicate that female T. tana are a mixture of philopatric residents and immigrants from other areas. Coalescent- based Bayesian analyses also show that historical female migration has been three times higher than the overall migration rate between primary and logged forest populations, providing evidence of female-biased gene flow. ASOCIAL MONOGAMY, EXTRA-PAIR PATERNITY, AND DISPERSAL IN THE LARGE TREESHREW (Tupaia tana) By Jason Munshi-South Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2006 Advisory Committee: Professor Gerald S. Wilkinson, Chair Professor Devra G. Kleiman, Co-Advisor Professor James M. Dietz Professor Robert Fleischer Professor Matthew P. Hare Professor David J. Hawthorne © Copyright by Jason Munshi-South 2006 Preface This dissertation contains a single introduction section and three chapters. Chapters I, II, and III are presented in manuscript form, with abstract, introduction, methods, results, and discussion, followed by tables, figure legends, and figures. A single appendix follows the chapters in the format in which it was published (Molecular Ecology Notes. 2006. in press). A single bibliography section occurs at the end for references cited throughout the dissertation. ii Dedication To Versha, with love iii Acknowledgements I would like to thank my dissertation advisors, Jerry Wilkinson and Devra Kleiman, for the freedom to pursue this project and excellent training in the scientific process. Jerry also largely turned a blind eye as I ran up a tab in his laboratory. This dissertation would not have been possible without the contributions of Louise Emmons, whose book on treeshrews was serendipitous. Tim Wright taught me how to do PCR and interpret genetic results, and Eduardo Eizirik provided the original pygmy treeshrew DNA sample for microsatellite development. Thank you to Oliver Schülke for providing his testis size data, and Rutger Vos for access to his primate supertree before it was published. I also owe thanks to my dissertation committee, the Wilkinson lab, Holly Menninger, Tagide DeCarvalho and Sheila Reynolds for their valuable comments on these chapters. The staff of the biology department, and the amazing Lois Reid in particular, also deserve recognition for their support. For their friendship, I thank the students in the BEES and Biology programs. I must thank the Economic Planning Unit of Malaysia, the Danum Valley Management Committee, the Sabah Wildlife Department, Prof. Rory Walsh, and PM Datin Dr. Maryati Mohamed for permission to work in such a wonderful place. The Institute for Tropical Biology and Conservation, U. Malaysia Sabah, the Royal Society Southeast Asia Rainforest Research Programme , and Dr. Edwin Bosi provided invaluable logistical support. Many thanks also to Dr. Henry Bernard and Glen Reynolds for their friendship and interest in my work. I could not imagine a better tour guide and friend than Adriene Leong, whose love for Malaysia is infectious. Noel Tawatao was a gracious host, and provided much moral support when I was confronted with the difficult aspects of working in a foreign country. I would like to thank Jo Annah Jensen, Kenny Johnius, Tracy Misiewicz, Ronie Sham, Philip Ulok, Raleigh International, and the staff of the Sabah Biodiversity Experiment for their heroic assistance in the field, and reminding me that I’m not nearly as tough as I think I am. Thank you to Aimee Sayer, Yuko Morimoto, Alex and Apek Karolus, Jamil Hanapi, Nasir Majid, Bakhtiar Effendi bin Yahya, Robert Bagchi, Johnny Larenus, Mike Bernadus Balaola, Jan and Nortasha Beck, Wani Oredi, Alex Dumbrell, Eleanor, Jerome, Chris, Sam, and Philip for cigarettes, beer, great conversation and camaraderie. A special thank you to my grandparents, Richard and Verna South and Joe and Joanne Seay, for passing on their love of nature, and to my parents for supporting all of my endeavors. Thank you to Versha Munshi-South, for everything. My research was financially supported by a Dean’s Dissertation Fellowship and grants from the American Society of Mammalogists, the Animal Behavior Society, the Biology of Small Populations RTG, the Cleveland Zoological Society, the Explorers Club Exploration Fund, Sigma Xi, and the University of Maryland Center for Biodiversity. iv Table of Contents Preface........................................................................................................................... ii Dedication....................................................................................................................iii Acknowledgements...................................................................................................... iv Table of Contents.......................................................................................................... v List of Tables .............................................................................................................. vii List of Figures............................................................................................................viii Introduction................................................................................................................... 1 Chapter I Behavioral monogamy and fruit availability in the large treeshrew (Tupaia tana).... 15 Abstract................................................................................................................... 15 Introduction............................................................................................................. 16 Methods................................................................................................................... 18 Results..................................................................................................................... 27 Discussion............................................................................................................... 31 Tables...................................................................................................................... 41 Figure legends......................................................................................................... 45 Figures..................................................................................................................... 47 Chapter II Extra-pair paternity in a behaviorally monogamous tropical mammal, the large treeshrew, (Tupaia tana) .............................................................................................................. 53 Abstract................................................................................................................... 53 Introduction............................................................................................................. 54 Methods................................................................................................................... 58 Results..................................................................................................................... 64 Discussion..............................................................................................................
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