Investigating the role of epigenetic variation in adaptive responses

Mark Smithson

The contribution of epigenetic modifications to variation in traits and fitness among populations is still largely unknown, but could significantly affect our understanding of adaptation, environmental change, and disease. We used a combination of empirical and theoretical approaches to investigate the role of epigenetic modifications in three general types of adaptive responses to environmental variation (adaptive within-generation plasticity, adaptive trans-generational plasticity, and responses to natural selection across generations). In chapter one, we used mathematical models and computer simulations to compare the effect of heritable genetic vs. epigenetic modifications on adaptation to local environmental conditions across generations. Our work advanced theory on the role of epigenetic variation in adaptive responses by considering the effect of epigenetic mutations on local adaptation in the context of migration, selection, and genetic drift. In chapter two, we tested whether between-habitat phenotypic variation in asexual New Zealand freshwater snails resulted from within-generation plasticity, trans-generation plasticity, or a response to selection across generations. We also measured habitat-specific differences in DNA methylation across generations. Our results suggested that adaptive phenotypic variation resulted from a transgenerational response to the environment, which was associated with stability in DNA methylation. This study provided the first evidence of stability of DNA methylation patterns across one generation in an asexual animal. In chapter three, we introduced a method, called MST, for quantifying the structure of epigenomic variation among populations from enrichment-based sequencing data, and discussed how the results could be used to probe links between specific epigenetic variants and phenotypic variation. As a proof of concept, we used the MST framework to quantify among-population structure of epigenomic and phenotypic variation within a single clonal lineage of the New Zealand freshwater snail. Higher structure between regions (Lake vs. river populations) than among populations suggested that methylation has either responded to divergent evolutionary forces across generations (e.g., genetic drift and selection) or local environments within generations. Taken together, our approach and results showed that analyzing epigenomic and phenotypic structure among populations provides a framework for assessing the contribution of epigenetic variation to trait variation.

Investigating the role of epigenetic variation in adaptive responses

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