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Primate Skeletal Epigenetics

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Primate Skeletal Epigenetics Primate Skeletal Epigenetics: Evolutionary Implications of DNA Methylation Patterns in the Skeletal Tissues of Human and Nonhuman Primates by Genevieve Housman A Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy Approved April 2017 by the Graduate Supervisory Committee: Anne Stone, Chair Ellen Quillen Kenro Kusumi Christopher Stojanowski ARIZONA STATE UNIVERSITY May 2017 ABSTRACT Within the primate lineage, skeletal traits that contribute to inter-specific anatomical variation and enable varied niche occupations and forms of locomotion are often described as the result of environmental adaptations. However, skeletal phenotypes are more accurately defined as complex traits, and environmental, genetic, and epigenetic mechanisms, such as DNA methylation which regulates gene expression, all contribute to these phenotypes. Nevertheless, skeletal complexity in relation to epigenetic variation has not been assessed across the primate order. In order to gain a complete understanding of the evolution of skeletal phenotypes across primates, it is necessary to study skeletal epigenetics in primates. This study attempts to fill this gap by identifying intra- and inter- specific variation in primate skeletal tissue methylation in order to test whether specific features of skeletal form are related to specific variations in methylation. Specifically, methylation arrays and gene-specific methylation sequencing are used to identify DNA methylation patterns in femoral trabecular bone and cartilage of several nonhuman primate species. Samples include baboons (Papio spp.), macaques (Macaca mulatta), vervets (Chlorocebus aethiops), chimpanzees (Pan troglodytes), and marmosets (Callithrix jacchus), and the efficiencies of these methods are validated in each taxon. Within one nonhuman primate species (baboons), intra-specific variations in methylation patterns are identified across a range of comparative levels, including skeletal tissue differences (bone vs. cartilage), age cohort differences (adults vs. juveniles), and skeletal disease state differences (osteoarthritic vs. healthy), and some of the identified patterns are evolutionarily conserved with those known in humans. Additionally, in all nonhuman primate species, intra-specific methylation variation in association with nonpathological i femur morphologies is assessed. Lastly, inter-specific changes in methylation are evaluated among all nonhuman primate taxa and used to provide a phylogenetic framework for methylation changes previously identified in the hominin lineage. Overall, findings from this work reveal how skeletal DNA methylation patterns vary within and among primate species and relate to skeletal phenotypes, and together they inform our understanding of epigenetic regulation and complex skeletal trait evolution in primates. ii ACKNOWLEDGMENTS I would like to thank my dissertation committee for their assistance during the development of my research, support during my data collection, and feedback during the final synthesis and writing of my dissertation. I want to specifically thank Lorena Havill for allowing me to initiate the baboon skeletal DNA methylation pilot project that started it all. Additionally, I am especially grateful to Ellen Quillen who granted me access to her lab and samples at the Texas Biomedical Research Institute and provided extremely helpful guidance during my data collection and analyses. I am also appreciative of Christopher Stojanowski and Kenro Kusumi for their helpful feedback and conversations. Lastly, I would like to express my immense gratitude to Anne C. Stone, my dissertation chair, for her constant support and guidance during my graduate student career. I would also like to express my gratitude to the many researchers at the Texas Biomedical Research Institute that granted me access to their facilities, resources, and samples. Additionally, this research would not have been possible without the skeletal remains of several nonhuman primates housed at the Texas Biomedical Research Institute. Finally, I would like to thank all the funding agencies that enabled this research – the Max and Minnie Tomerlin Voelcker Foundation, the William and Ella Owens Foundation for Biomedical Research, the Southwest National Primate Research Center, Sigma Xi, the Leakey Foundation, the Wenner-Gren Foundation [Gr. 9310], the Nacey Maggioncalda Foundation, the International Primatological Society, the Center for Evolution and Medicine at ASU, the Graduate Research and Support Program at ASU, and the School of Human Evolution and Social Change at ASU. iii I would also like to thank my fellow labmates in the Molecular Anthropology Laboratory and specifically María A. Nieves-Colón and Tanvi Honap for their assistance, encouragement, and friendship while we navigated through the highs and lows of academia together, taught ourselves to be bioinformaticians, and pushed each other to be amazing scientists. I am also grateful to my other fellow doctoral students for their willingness to help and support me regardless of my divergent epigenetic interests. Specifically, to John Rowan and Kathleen Paul, thank you for your friendship and for making sure I stayed somewhat involved in social activities, and to Halszka Glowacka, thank you for being an amazing roommate and helping me to find nonacademic activities that kept me healthy and strong throughout my dissertation. Last but certainly not least, I am eternally grateful to my closest friends and family for their never-ending support of me and my academic pursuits. Specifically, to my parents, Jeanne Bowen and David Housman, thank you for your love and encouragement through all my research endeavors and my life in general. Finally, to Eric D. Johnson, thank you for everything that you have done to help me during this process, from bringing me dinner on the many occasions I worked late into the night on campus to guiding me in the development of a massive relational database, teaching me more efficient research workflow pipelines, and helping me understand complicated statistical analyses. You pushed me to think critically about my research, and our discussions have helped me to become a better scientist, educator, and human. I cannot thank you enough. Beyond this, I am indebted to so many other people that have helped me to get to this point in my career and life. This includes my primary and secondary educators, my first research supervisor during my undergraduate education, Sibaji Sarkar, and numerous iv other faculty, staff members, colleagues, and associates that have helped me along my journey. I apologize if I forgot to mention anyone, but please know, I am eternally grateful for your support. v TABLE OF CONTENTS Page LIST OF TABLES ................................................................................................................ xiii LIST OF FIGURES ................................................................................................................ xv LIST OF EQUATIONS ......................................................................................................... xix CHAPTER 1 INTRODUCTION ...................................................................................................... 1 2 ASSESSMENT OF DNA METHYLATION PATTERNS IN THE BONE AND CARTILAGE OF A NONHUMAN PRIMATE MODEL OF OSTEOARTHRITIS .................................................................................................. 5 Abstract ................................................................................................................... 5 Key Words .............................................................................................................. 6 Introduction ............................................................................................................ 6 Methods .................................................................................................................. 9 Results .................................................................................................................. 18 Discussion ............................................................................................................. 24 Acknowledgements .............................................................................................. 30 Funding ................................................................................................................. 30 3 AN EVOLUTIONARY PERSPECTIVE OF DNA METHYLATION PATTERNS IN SKELETAL TISSUES USING A NONHUMAN PRIMATE MODEL OF OSTEOARTHRITIS ........................................................................... 31 Abstract ................................................................................................................. 31 Key Words ............................................................................................................ 32 vi CHAPTER Page Introduction .......................................................................................................... 32 Methods ................................................................................................................ 35 Results .................................................................................................................. 46 Discussion ............................................................................................................. 72 Acknowledgements .............................................................................................
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