Browsing by Author "Tung, Jenny"

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 three major themes: (i) the adaptive significance of early life effects, (ii) the molecular mechanisms that connect early life experiences with later life traits, and (iii) the development of laboratory tools 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 long-lived species. In chapter two, I address the degree to which ecological effects on fitness-related traits 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 work provides some of the first empirical data on the genes and mechanisms involved in sensing and responding to environmental variation in wild mammals, and more generally addresses several critical gaps in our understanding of how early experiences affect evolutionarily relevant traits.

Changes in gene regulation are thought to play an important role in primate evolution and divergence. In support of this hypothesis, comparative evidence clearly demonstrate that gene expression patterns differ between closely related species and tend to evolve under selective constraint. However, we know little about the evolutionary forces that shape gene regulation across primates, particularly outside of humans and the other great apes. To address this gap, my dissertation draws on population and functional genomic variation between baboon species and within an admixed wild baboon population to address two themes: (i) how is gene regulatory divergence related to genetic divergence? and (ii) to what extent has natural selection shaped regulatory variation? Using interspecific comparative approaches, I show that changes in DNA methylation accumulate with increasing sequence divergence. While most changes in methylation can be explained by genetic drift, a subset are likely to have evolved under positive selection. Then, using genomic data from admixed baboons, I show that interspecific changes in DNA methylation are linked to genetic effects on DNA methylation (i.e., methylation quantitative trait loci, meQTL) and differences in allele frequency between baboon species. I also show that changes in DNA methylation are associated with changes in gene expression. Finally, I identify genomic evidence for selection against admixture in baboons, especially near genes that are differentially expressed between species. Together, my work highlights the close relationship between genetic and gene regulatory divergence in baboons. It also emphasizes the importance of natural selection in shaping genetic and regulatory variation throughout primate evolution, including in a living model for admixture in our own lineage.

Although evolution results from differential reproduction and survival at the level of the individual, most research in evolutionary genetics is concerned with comparisons made at the level of divergent populations or species. This is particularly true in work focused on the evolutionary genetics of natural populations. While this level of inquiry is extremely valuable, in order to develop a complete understanding of the evolutionary process we also need to understand how traits evolve within populations, on the level of differences between individuals, and in the context of natural ecological and environmental variation. A major difficulty confronting such work stems from the difficulty of assessing interindividual phenotypic variation and its sources within natural populations. This level of inquiry is, however, the main focus for many long-term field studies. Here, I take advantage of one such field study, centered on the wild baboon population of the Amboseli basin, Kenya, to investigate the possibilities for integrating functional, population, and evolutionary genetic approaches with behavioral, ecological, and environmental data. First, I describe patterns of hybridization and admixture in the Amboseli population, a potentially important component of population structure. Second, I combine field sampling, laboratory measurements of gene expression, and a computational approach to examine the possibility of using allele-specific gene expression as a tool to study functional regulatory variation in natural populations. Finally, I outline an example of how these and other methods can be used to understand the relationship between genetic variation and naturally occurring infection by a malaria-like parasite, Hepatocystis, also in the Amboseli baboons. The results of this work emphasize that developing genetic approaches for nonmodel genetic systems is becoming increasingly feasible, thus opening the door to pursuing such studies in behavioral and ecological model systems that provide a broader framework for genetic results. Integrating behavioral, ecological, and genetic perspectives will allow us to better appreciate the interplay between these different factors, and thus achieve a better understanding of the raw material upon which selection acts.

Hybridization, the process of interbreeding between distinct taxa, was once thought to be rare in animals. However, in the past two decades, new data have challenged this paradigm. Ancient and/or ongoing hybridization has now been documented in a wide variety of animals, including in our own lineage. A key puzzle that emerges from these observations is that despite the pervasiveness of hybridization, many species nevertheless remain distinct. My dissertation addresses this puzzle by integrating long-term field data on morphology, behavior, demography, and ecology with newly generated genomic data from a natural hybrid zone between yellow baboons (Papio cynocephalus) and anubis baboons (P. anubis) in Kenya.

My work addresses three main themes: (i) the effects of ancestry on fitness-related traits in hybrid zones; (ii) the role of behavior in mediating gene flow between species; and (iii) the genomic signature of natural selection post-hybridization. I show that genetic ancestry predicts male-female social bonds, a predictor of lifespan in this population. Animals with more introgressed ancestry (i.e., genetic regions transferred via hybridization) are more likely to affiliate with the opposite sex, and pairs of animals with similar ancestry show an increased propensity for affiliation. These findings suggest that affiliative behavior may simultaneously promote and constrain baboon hybridization, through additive and assortative effects of ancestry, respectively. My research also rules out the possibility that fetal loss—a major cost to female fertility—acts as a strong isolating barrier. Fetal loss is independent of maternal genetic ancestry; instead, age and ecological stressors are the main determinants of pregnancy outcomes in baboons. Notably, although these analyses fail to identify clear costs to hybrid ancestry, population genomic evidence points to selection against introgression in baboons, suggesting subtle but important phenotypic effects of ancestry that have yet to be revealed. Finally, I identify specific regions of the baboon genome that may serve as barriers to gene flow. A subset of these genomic regions may explain ancestry-based assortative mating behavior in the hybrid zone. Together, my work demonstrates how hybridization has shaped the genomes and phenotypes of interbreeding baboons. It also provides a much-needed comparative perspective against humans, illuminating the shared and distinctive features of admixture as an evolutionary process in human evolution, and more broadly reveals how primates fit into our changing concept of animal evolution more broadly.

The environment dictates many facets of animals’ lives, including how long individuals live and their physiology, fertility, and health along the way. While environment-responsive changes in gene regulation likely play a role in this relationship, we rarely have a clear understanding of the socioenvironmental determinants of gene regulation in natural primate populations. My dissertation addresses this gap by linking longitudinal observations of environmental experiences to measures of gene regulation in wild baboons from a long-term field study in Kenya. By adopting a genome-scale perspective, I investigate (i) whether distinct environmental stressors are reflected in distinct changes in gene regulation, and whether there are sex differences in these relationships, and (ii) what pathways are sensitive to environmental adversity, and whether these pathways overlap across different sources of stress. In chapter one, I test whether environmental stressors accelerate the aging process. I show that, according to a DNA methylation-based “epigenetic clock,” high ranking males experience accelerated aging. In chapter two, I test for links between variation in the adult social environment (social status and social bond strength) and blood-based gene expression. I demonstrate that dominance rank in male and female baboons has directionally opposite links to gene regulation, and that social bonds uniquely predict a more robust response to simulated bacterial threat. In chapter three, I systematically test the hypothesis that biological embedding via DNA methylation translates early life experience into lasting phenotypic effects in adulthood. I find widespread, and often overlapping, associations between major sources or early life adversity and DNA methylation measured in adulthood. Taken together, my work underscores the close ties between fitness-relevant environments and gene regulation in wild primates, including the existence of some pathways that are broadly sensitive to multiple types of environmental stressors. These contributions help fill important gaps in our understanding of the complex mechanisms that connect socioenvironmental variation, phenotype, and evolution in the primate lineage.