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Preliminary Pages 2013 Alison Golinski Goldberg ALL RIGHTS RESERVED EVOLUTIONARY PLASTICITY IN THE PLEIOTROPIC REGULATION OF SEXUALLY DIMORPHIC TRAITS IN GEKKOTAN LIZARDS by ALISON GOLINSKI GOLDBERG A Dissertation submitted to the Graduate School-New Brunswick Rutgers, The State University of New Jersey in partial fulfillment of the requirements for the degree of Doctor of Philosophy Graduate Program in Endocrinology and Animal Biosciences written under the direction of Dr. Henry B. John-Alder and approved by ________________________ ________________________ ________________________ ________________________ ________________________ New Brunswick, New Jersey May 2013 ABSTRACT OF THE DISSERTATION Evolutionary Plasticity in the Pleiotropic Regulation of Sexually Dimorphic Traits in Gekkotan Lizards By ALISON GOLINSKI GOLDBERG Dissertation Director: Dr. Henry B. John-Alder Sexually dimorphic traits evolve due to selection for reproductive advantage, and their expression is often functionally correlated by the pleiotropic effects of gonadal steroids (e.g., testosterone, T, in males). When T mediates the correlated expression of traits, then how can changes in individual traits evolve? The main objective of this dissertation was to investigate whether circulating T or androgen receptors in the brain underlie sex- and species-differences in sexually dimorphic trait expression in a comparative study of three species of gekkotan lizards (Goniurosaurus lichtenfelderi, Coleonyx elegans, and Paroedura picta). I hypothesized sex differences in trait expression are due to differences in circulating T, and that the absence of various traits in C. elegans and P. picta are due to a specific alteration in the androgen signaling system rather than a reduction in T. I conducted surgical manipulations to alter levels of T in adult males and females of each species. Testosterone-sensitive traits included courtship, copulatory mounting, and aggressive behaviors, secretions from precloacal pores, enlargement of the hemipenes and head width. Elevated T in males was almost always the primary mediator of sex differences in trait expression within species. Some, but not ii all, of the male-typical traits were induced in adult females, suggesting the neural or physiological substrates underlying certain traits are permanently differentiated between the sexes prior to adulthood. Traits absent from the phenotype of a species, such as courtship in C. elegans and P. picta, cannot be induced by exogenous T. I hypothesized differences in behavioral sensitivity to T would be due to differences in androgen receptors in brain regions associated with control of reproductive behaviors. Immunohistochemistry revealed P. picta had increased abundance of androgen receptor immunoreactivity (AR-ir) in the preoptic area and ventromedial hypothalamus relative to G. lichtenfelderi. Thus, the abundance of AR-ir does not reflect the expression of courtship and aggressive behaviors in these species. Although circulating T or AR-ir do not explain interspecific differences in trait expression, results indicate that correlated traits are not constrained by the pleiotropic effects of T but targeted changes in sensitivity to T allows evolutionary diversification of trait expression. iii DEDICATION To all the teachers in my life, who have set me on this path to accomplish my goals. iv ACKNOWLEDGEMENTS First, I would like to thank my mentor and advisor, Dr. Henry B. John-Alder, for supporting my academic and professional development. I deeply respect Henry and am very grateful for the many lessons he taught me, especially the importance of understanding the science behind the protocol, patience in the lab, reading critically and the value of writing and re-writing multiple drafts. Henry also introduced me to the unique opportunities associated with scientific collaborations. Next, I must thank the members of my committee. Dr. Mike Sukhdeo provided his ecological and evolutionary insights. Dr. Nina Fefferman gave me much needed guidance on mathematical techniques to tackle analysis of complicated and voluminous behavioral data. I also want to thank Nina for her words of encouragement and friendly smile. I thank Dr. Carol Bagnell and members of her lab for providing training in molecular biology techniques. In addition, it was very kind of Carol to offer space in her own laboratory so that I could conduct Western blots. I would like to thank my outside committee member Dr. Juli Wade, who is a leader in the field of behavioral neuroendocrinology. I highly value Juli’s insight and I thank her for contributing to my development as a scientist. I also thank Juli and members of her laboratory at Michigan State University for welcoming and teaching me how to process lizard tissue samples for histology and molecular assays. I am grateful for the years spent in the John-Alder laboratory with my former lab mates Christine Duncan and Marisol Gutierrez. Graduate school is a uniquely challenging experience, and having a supportive network of friends with shared interests and experiences was both helpful and enriching. I am also fortunate to have had the v opportunity to work with some wonderful undergraduate students, including Tracy Brynildsen and Daria Pazdzior, who were enthusiastic and motivated. I would like to extend my gratitude to everyone in the Department of Animal Sciences, which provided an environment that facilitated my professional growth and development. I would like to specifically recognize Kathy Manger for her encouragement and sincere interest in the progress and ongoing success of students. I would like to gratefully acknowledge my collaborators at Charles University in Prague, Czech Republic. Drs. Lukáš Kratochvíl, Lukáš Kubička, and Zuzana Starostová welcomed me into their laboratory for months at a time, shared their scientific perspective and their culture. Děkuji moc! My dissertation research would not have been possible without funding from the School of Environmental and Biological Sciences, Fulbright, and the Central Europe Summer Research Institute, sponsored by the National Science Foundation and the Institute of International Education. I am thankful for the professors who introduced me to biological research while an undergrad at Rider University. I must acknowledge Drs. Laura Hyatt, Paul Jivoff, Gabriela Smalley and the late Dr. Richard Alexander. I could never thank my family enough for their encouragement and support, especially my Mom, Dad, brother, sister-in-law and niece. And finally, I thank my husband, whose unceasing support gave me the confidence, fortitude, and determination to earn my Ph.D. vi TABLE OF CONTENTS Title Page................................................................................................................... i Abstract..................................................................................................................... ii Dedication................................................................................................................. iv Acknowledgements................................................................................................... v Table of Contents...................................................................................................... vii List of Tables............................................................................................................. xi List of Illustrations..................................................................................................... xii List of Abbreviations................................................................................................. xiv CHAPTER 1. Introduction Questions regarding the evolution of sexually dimorphic traits................... 1 Hormonal pleiotropy and the androgen control module............................... 3 Gecko lizard model system........................................................................... 5 Androgen-mediated suites of traits in male vertebrates................................ 9 Specific aims of this dissertation................................................................... 15 References...................................................................................................... 16 Figures........................................................................................................... 27 CHAPTER 2. Effects of Testosterone on the Expression of Sexually Dimorphic Traits in the Yucatan Banded Gecko (Eublepharidae: Coleonyx elegans) Abstract......................................................................................................... 30 Introduction................................................................................................... 31 vii Methods......................................................................................................... 33 Results ........................................................................................................... 40 Discussion..................................................................................................... 44 References..................................................................................................... 52 Tables............................................................................................................ 55 Figures........................................................................................................... 57 CHAPTER 3. Effects of Testosterone on the Expression of Sexually Dimorphic Traits in Lichtenfelderi’s
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