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By Amanda Jeanne Lea University Program in Ecology D Evolution and Mechanisms of Plasticity in Wild Baboons (Papio cynocephalus) by Amanda Jeanne Lea University Program in Ecology Duke University Date:_______________________ Approved: ___________________________ Jenny Tung, Co-supervisor ___________________________ Susan Alberts, Co-supervisor ___________________________ Anne Pusey ___________________________ Barbara Engelhardt Martin ___________________________ Susan Murphy Dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the University Program in Ecology in the Graduate School of Duke University 2017 ABSTRACT Evolution and Mechanisms of Plasticity in Wild Baboons (Papio cynocephalus) by Amanda Jeanne Lea University Program in Ecology Duke University Date:_______________________ Approved: ___________________________ Jenny Tung, Co-supervisor ___________________________ Susan Alberts, Co-supervisor ___________________________ Anne Pusey ___________________________ Barbara Engelhardt Martin ___________________________ Susan Murphy An abstract of a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the University Program in Ecology in the Graduate School of Duke University 2017 Copyright by Amanda Jeanne Lea 2017 Abstract In many species, early life experiences have striking effects on health, reproduction, and survival in adulthood. Thus, early life conditions shape a range of evolutionarily relevant traits, and in doing so alter the genotype-phenotype relationship and the phenotypic distribution on which selection acts. Because of the key role early life effects play in generating variation in fitness-related traits, understanding their evolution and mechanistic basis is crucial. To gain traction on these topics, my dissertation draws on ecological, demographic, and genomic data from a long-term study population of wild baboons in Amboseli, Kenya to address two themes: (i) the adaptive significance of early life effects and (ii) the molecular mechanisms that connect early life experiences with later life traits. In service to the second theme, I also (iii) develop a laboratory method for understanding the role of one particular mechanism— DNA methylation—in translating environmental inputs into phenotypic variation. In chapter one, I empirically test two competing explanations for how early life effects evolve, providing novel insight into the evolution of developmental plasticity in a long- lived species. In chapter two, I address the degree to which ecological effects on fitness- related traits in a wild baboon population are potentially mediated by changes in DNA methylation. Finally, in chapter three, I develop a high-throughput assay to improve our knowledge of the phenotypic relevance of changes in the epigenome. Together, this iv work provides insight into the genes and mechanisms involved in sensing and responding to environmental variation, and more generally addresses several key gaps in our understanding of how environmental inputs are translated into evolutionarily relevant trait variation. v Contents Abstract ......................................................................................................................................... iv List of Tables .................................................................................................................................. xi List of Figures .............................................................................................................................. xii Acknowledgements ................................................................................................................... xiii 1. Introduction ................................................................................................................................ 1 1.1 Background ........................................................................................................................ 1 1.2 Chapter 1: The adaptive significance of developmental plasticity ............................ 3 1.2.1 Key questions and current gaps in knowledge ....................................................... 3 1.2.2 Empirical tests of developmental constraints versus predictive response models ..................................................................................................................................... 6 1.3 Chapter 2: The molecular mechanisms that mediate developmental plasticity ...... 8 1.3.1 Key questions and current gaps in knowledge ....................................................... 8 1.3.2 Environmental effects on the epigenome in natural populations ...................... 11 1.4 Functional effects of variation in DNA methylation ................................................. 13 1.4.1 Key questions and current gaps in knowledge ..................................................... 13 1.4.2 Methods for causally testing the effects of DNA methylation on gene expression ............................................................................................................................. 15 2. Developmental constraints in a wild primate ..................................................................... 18 2.1 Introduction ..................................................................................................................... 18 2.2 Materials and Methods ................................................................................................... 24 2.2.1 Study subjects, fertility data, and social status data ............................................. 24 vi 2.2.2 Rainfall data and the 2009 drought ......................................................................... 25 2.2.3 Defining low-quality environments in early life and adulthood ........................ 25 2.2.4 Defining high-quality environments in early life and adulthood. ..................... 27 2.2.5 Within-female analyses: interaction between early life and adult conditions on female fertility ..................................................................................................................... 27 2.2.6 Between-condition analyses: testing for early life effects on adult fertility in a given adult environment ................................................................................................... 30 2.2.7 Sensitivity to low and high rainfall in early life and adulthood ......................... 31 2.2.8 Effects of maternal dominance rank on female fertility ....................................... 32 2.3 Results ............................................................................................................................... 34 2.3.1 Fertility declines during the 2009 drought were greater for females born in low-quality environments than for females born in high-quality environments ...... 34 2.3.2 Sensitivity of female fertility to both extreme low and extreme high rainfall .. 38 2.3.3 Protective effects of high social status in early life ............................................... 41 2.4 Discussion ........................................................................................................................ 42 2.4.1 Support for the developmental constraints model in wild baboons .................. 42 2.4.2 Factors that influence the relationship between early life ecology and adult fertility .................................................................................................................................. 45 2.4.3 Conclusions ................................................................................................................. 47 3. Resource base influences genome-wide DNA methylation levels in wild baboons ..... 49 3.1 Introduction ..................................................................................................................... 49 3.2 Materials and methods ................................................................................................... 54 3.2.1 Study subjects and sample collection ...................................................................... 54 vii 3.2.2 Generation and processing of genome-wide DNA methylation data ............... 56 3.2.3 Testing for differences in DNA methylation levels at individual CpG sites .... 58 3.2.4 Enrichment of differentially methylated sites by genomic annotation .............. 59 3.2.5 Testing for differences in DNA methylation levels at metabolic pathways ..... 62 3.2.6 Identification of differentially methylated regions (DMRs) ................................ 63 3.2.7 Testing the effects of PFKP promoter methylation on gene expression levels . 63 3.2.8 Investigating the stability or plasticity of DNA methylation levels for individuals that switched between resource bases ........................................................ 65 3.3 Results ............................................................................................................................... 67 3.3.1 Genome-wide DNA methylation levels contain a signature of resource base . 67 3.3.2 Sites associated with resource base are enriched in functionally important regions of the genome ........................................................................................................ 69 3.3.3 Resource base-associated CpG sites are enriched in specific biological pathways .............................................................................................................................. 70 3.3.4 DMRs occur more often than expected
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