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BEHAVIORAL AND GENETIC CORRELATES OF REPRODUCTIVE SUCCESS IN MALE ADDAX (ADDAX NASOMACULATUS, DE BLAINVILLE 1816) BY EDWARD M. SPEVAK DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology with a concentration in Ecology, Ethology, and Evolution in the Graduate College of the University of Illinois at Urbana-Champaign, 2015 Urbana, Illinois Doctoral Committee: Professor Kenneth Paige, Chair, Director of Research Professor Andrew Suarez Professor C.-H. Christina Cheng Associate Professor Alfred Roca ABSTRACT The addax (Addax nasomaculatus) is a critically endangered antelope whose range is now restricted to a few small populations in the Sahara and thus the focus of national and international conservation efforts. Very little is known about their general behavior and social structure, either in the wild or in captivity. This study examined the behavior of semi-free ranging herds of addax to establish the mating strategies male addax pursue to increase their reproductive success. This study demonstrates that addax have the ability to become territorial under certain conditions, possibly due to the high population density and constant resource base as seen in related oryx species. Two mating strategies were evident among male addax in this population: territorial and following or non-territorial. Resources and the behavior and density of females influenced the presence of these different mating strategies with male age and rank and available territory determining the strategy. Male reproductive success of addax was assessed using both behavioral observations and genetic paternity analysis using microsatellites and the second exon of Adna DR3 of the major histocompatibility complex (MHC). There was a significant relationship between the age of the male and the number of offspring sired (rs =.46, N = 66, p = .0002) and a male's rank and his reproductive success (rs = -.88, p = .0007). There was no difference between the total number of calves sired by territorial versus non-territorial males. However, individual territorial males sired on average significantly more calves than non-territorial males. Possession 2 of a territory was a significant component of reproductive success (R = .27, F.05= 11.77, d.f. = 2, 63, p < .05). There was a significant difference between behavioral and genetic estimates with behavioral data overestimating the reproductive success of younger age classes (1-2 year olds and 2-3 year olds) and underestimated the 3 year olds and above. In this study, comparisons between genetic and behavioral estimates of reproductive success showed that behavioral estimates consistently underestimated the absolute reproductive success of successful males and overestimated the success of many unsuccessful males. However, in the absence of known paternity behavioral methods give an adequate estimate of male reproductive success for multi- male herds. This is the first study of addax in which territorial behavior was observed and where its benefits, in terms of reproductive success, were assessed. This study also demonstrates the usefulness of microsatellites and DRB3 of the MHC in helping to establish paternity and ii therefore reproductive success in addax. Additionally, a further examination of Adna DRB3 of the MHC found low levels of allelic diversity in addax. Despite low levels of allelic diversity, as measured by DR measures of heterozygosity within and among addax populations were found to be informative, correlating highly with infant survivorship and average heterozygosity across the genome as measured using microsatellite markers. iii ACKNOWLEDGMENTS So many people contributed in so many ways towards the development, execution, and final completion of this project. I would especially like to thank my third and final graduate advisor, Dr. Ken Paige, who took me on as his first graduate student and has put up with me these many years hoping that I would complete my dissertation. He has been the best advisor a student could ever ask for. He has been a good friend and colleague, without whose support, enthusiasm, and humor I could never have finished. This research could never have been done without the support, staff, facilities, and addax of the Fossil Rim Wildlife Center and Fossil Rim Wildlife Foundation. To the late Jim Jackson and Christine Jurzykowski who gave me support, a home, and family in one of the most beautiful spots on earth. Also to Dr. Evan Blumer, a good friend and colleague, who was instrumental in getting me to Fossil Rim and getting me started and who worked closely with me on the setup of this research project. To Adam Eyres, Rodney Marsh, Kelly Snodgrass and Bruce Williams who supplied me with more than ample amounts of friendship and good times and who cared about the addax as much as I did. To Drs. Evan Blumer, Tom Demar and Steve Osofsky for drawing countless tubes of blood and Cathy Thurman for packing and shipping blood and tissue samples to me in the lab. Also to Rebecca Christie and Peg Gronemeyer for keeping an eye on my addax while I was away from Fossil Rim and keeping me informed about their daily lives. I would like to thank the late Dr. Tom Foose for his initial faith in me and for recommending me to the Addax Species Survival Plan (SSP) that I be the one to undertake and complete this research. Also to Terrie Correll who helped me piece together the history of the captive addax population and Dr. Robert Lacy for guidance. iv To Dr. Harris Lewin and the members of his lab Drs. John Beever, Michiel van Eijk, and Runlin Ma for introducing me to the major histocompatibility complex (MHC) and the beauty of its uses and information contained therein and how to run the lab tests to bring out the information. I would like to thank the Brookfield Zoo, Cheyenne Mountain Zoo, Henry Doorly Zoo, Fossil Rim Wildlife Center, Louisville Zoo, Miami Metro Zoo, Oklahoma City Zoo, San Antonio Zoo, San Diego Wild Animal Park, and the Saint Louis Zoo for supplying me with the blood and tissue samples to complete the project. To the Denver Zoological Society for providing me with additional financial support for lab equipment and supplies. I would like to thank my first advisor, Dr. Michael Lynch, for giving me my first “home” at the University of Illinois- Urbana Champaign and to my second advisor, the late Dr. M. Raymond Lee, who gave me another “home”, support, and laughter when this project began. To Drs. Christine Spolsky and Tom Uzzell for allowing me to use their lab in the startup of this project and to Dr. Chris Phillips for his humor and his initial guidance in my lab work. To Drs. Jim Jacobson and John Patton for collecting many of the initial blood samples and introducing me to new methods of DNA extraction and to the potential benefits of PCR. I would also especially like to thank one woman who was instrumental in helping me start and complete this research. To my wife and best friend Mary Brong for encouraging me to go back to grad school, for always being there in the beginning and knowing that I could do it, and for being there at the end. v TABLE OF CONTENTS CHAPTER 1: INTRODUCTION ....................................................................................................1 CHAPTER 2: MATING STRATEGIES OF MALE ADDAX (Addax nasomaculatus): DOMINANCE AND TERRITORIALITY ................................................................................4 CHAPTER 3: A COMPARISON OF GENETIC AND BEHAVIORAL ESTIMATES OF REPRODUCTIVE SUCCESS IN MALE ADDAX ................................................................23 CHAPTER 4: LOW GENETIC VARIABILITY AT MHC LOCUS Adna DR3 AND FITNESS IN ADDAX (Addax nasomaculatus) .......................................................................................47 CHAPTER 5: CONCLUSION .......................................................................................................57 FIGURES AND TABLES .............................................................................................................60 BIBLIOGRAPHY ..........................................................................................................................90 APPENDIX A ..............................................................................................................................124 APPENDIX B ..............................................................................................................................127 APPENDIX C ..............................................................................................................................129 APPENDIX D ..............................................................................................................................134 APPENDIX E ..............................................................................................................................138 vi CHAPTER 1: INTRODUCTION The addax (Addax nasomaculatus) is a critically endangered antelope whose range is now restricted to a few populations in the Sahara. Addax are probably the most desert-adapted of all the antelopes and now one of the most endangered. They formerly ranged across the Sahara from Egypt in the east to the Rio de Oro and Senegambia in the west (Dolan, 1966; Haltenorth and Diller, 1980; Harper, 1945). However, they have been exterminated over most of their range (Harper, 1945; Newby, 1980, 1984; UNEP/CMS 2006; Durant et al., 2014) due predominantly to hunting and poaching (Newby 1980, 1990), along with habitat loss, and
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