Behavior, Ecology and Genetics of Geoffroy's Tamarin (Saguinus geoffroyi) by Samuel Luis Díaz-Muñoz A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor in Philosophy in Integrative Biology in the Graduate Division of the University of California, Berkeley Committee in charge: Professor Eileen A. Lacey, Chair Professor Craig Moritz Professor Justin S. Brashares Spring 2010 Behavior, Ecology and Genetics of Geoffroy's Tamarin (Saguinus geoffroyi) Copyright © 2010, Some Rights Reserved (See: Appendix 1) Samuel Luis Díaz-Muñoz Abstract Behavior, Ecology and Genetics of Geoffroy's Tamarin (Saguinus geoffroyi) by Samuel Luis Díaz-Muñoz Doctor of Philosophy in Integrative Biology University of California, Berkeley Professor Eileen A. Lacey, Chair Cooperative behavior in reproductive contexts is rare among animals, especially males. Tamarins exhibit a rare breeding system called cooperative polyandry, in which a single breeding female mates with two or more males to produce fraternal twins and the males cooperate in caring for the infants by carrying young for the first 10 weeks of their lives. This peculiar breeding system raises questions about the adaptive consequences of male behavior. The nature of the breeding system also prompts questions about the ecological context and genetic consequences of this social organization. My research attempted address fundamental questions in behavior, ecology and evolutionary biology through the lens of individual behavior. Tamarins oftentimes inhabit disturbed habitats, however detailed space use within fragmented habitats is not well characterized. I used fine scale spatial and behavioral data in order to quantify habitat preference of S. geoffroyi in a heterogenous urban-forest landscape in central Panama. Using home range- based analyses and a novel method, first passage time analysis, I showed that tamarins spend significantly more time in secondary forest habitat and are more likely to forage and engage in social behavior in forest as compared to human-modified habitats. I examined the role of two aquatic barriers of varying age in creating population genetic structure in S. geoffroyi. I found that there was significant population differentiation across the Chagres River, an older, established riverine barrier and smaller, but detectable population structure across the Panama Canal, a recent anthropogenic riverine barrier. Finally, I examined the possible adaptive benefits of cooperative male parental care using genetic analyses of paternity and relatedness. I found that males in a group are often related and that they share paternity over multi-year associations. My results suggest that indirect and direct fitness benefits may play a role in maintaining male-male cooperation in tamarins. 1 I dedicate this dissertation to my mother, Carmen Rita Muñoz Berríos, for giving me life and never doubting me. Dedico este trabajo a mi madre, Carmen Rita Muñoz Berríos, por darme vida y nunca dudar que este día llegaría. i CONTENTS Contents.............................................................................................................................................................. ii Acknowledgements.......................................................................................................................................... iii Introduction....................................................................................................................................................... v Chapter 1............................................................................................................................................................ 1 Fine Scale Movement Analysis Reveals Preference for Forest in a Disturbance-tolerant Primate (Saguinus geoffroyi) in an Urban-forest Matrix........................................................................................... 1 Abstract.................................................................................................................................................... 1 Introduction............................................................................................................................................ 1 Methods................................................................................................................................................... 2 Results...................................................................................................................................................... 6 Discussion................................................................................................................................................ 8 Acknowledgments................................................................................................................................ 10 Literature Cited..................................................................................................................................... 11 Chapter 2.......................................................................................................................................................... 23 The role of riverine barriers in fine scale population genetic structure of Geoffroy's Tamarin (Saguinus geoffroyi) in the Panama Canal Watershed.............................................................................. 23 Abstract.................................................................................................................................................. 23 Introduction.......................................................................................................................................... 23 Methods................................................................................................................................................. 25 Results.................................................................................................................................................... 28 Discussion............................................................................................................................................. 29 Acknowledgments................................................................................................................................ 31 Literature Cited..................................................................................................................................... 32 Chapter 3.......................................................................................................................................................... 47 Male Cooperation in Polyandrous Geoffroy’s Tamarins ( Saguinus geoffroyi): Kinship and Paternity ..................................................................................................................................................... 47 Abstract.................................................................................................................................................. 47 Introduction.......................................................................................................................................... 47 Methods................................................................................................................................................. 48 Results.................................................................................................................................................... 51 Discussion............................................................................................................................................. 53 Acknowledgments................................................................................................................................ 55 Literature Cited..................................................................................................................................... 56 Appendix 1....................................................................................................................................................... 67 Copyright addendum: Creative Commons License............................................................................. 67 ii ACKNOWLEDGEMENTS This work would have not been possible without the aid of a large group of people throughout the years when I conducted my doctoral studies. Following is an attempt to thank most people who contributed in one way or another to this endeavor: First and foremost, I owe a huge debt of gratitude to my advisor and mentor, Dr. Eileen A. Lacey. She is an exceptional teacher, mentor and advisor for whom I have the highest regard. She encouraged me from the initial stages of my research to be independent and think big. Even though she was initially hesitant to have me study primates, once I convinced her of the opportunities in the study of Callitrichines, she was supportive and helpful in all stages. Eileen is an excellent editor and it is –in no small part – due to her assistance in crafting numerous grant applications that I was able to fund this project from the ground up. Eileen was active in providing suggestions throughout the project and was a source of comfort, encouragement and advice when things did not go the expected way. In the final stages she was instrumental in editing the dissertation and the manuscripts for publication. She provided the big picture and the significance of my findings (always emphasizing the biology of the organisms) at a time when