DNA methylation as an intra- and transgenerational mediator of phenotypic response

Abstract

The evolution of plasticity and its role in how species will evolve and adapt to shifting environments under global climate change is an area of on-going debate. To add to the complexity of this discussion, there is growing evidence that parental exposure to conditions predicted under climate change can affect offspring phenotype. A phenomenon known as transgenerational plasticity. My dissertation approaches this discussion from two perspectives; first, a molecular approach aimed at investigating the specific mechanisms that may be mediating both intra- and transgenerational plasticity in response to global climate change. Second, a theoretical modelling approach aimed at identifying the environmental conditions in which transgenerational plasticity is predicted to evolve. In chapter one, I examined the potential role of DNA methylation, an epigenetic modification, on the regulation of gene expression and biomineralization-related traits in the Eastern oyster (Crassostrea virginica) exposed to ocean acidification (OA). I found C. virginica had a short-term (9 day) capacity to respond to OA by maintaining the pH of their extra-pallial fluid (the site of calcification) despite the surrounding seawater being highly acidic, but this maintenance was not sustained for the full length of the exposure (80 days). The maintenance of the extra-pallial fluid corresponded to subtle shifts in both genome-wide DNA methylation and gene expression, but I observed little evidence of differential expression or methylation within specific genes. These results suggest the molecular response to OA in C. virginica may be largely canalized or regulated by a highly complex and polygenic architecture. In chapter two, I used an expanded animal model to investigate how different sources of variation (genetic and non-genetic) explain larval growth rate variance in C. virginica exposed to OA. This research built on a previous intergenerational exposure experiment, whereby adult C. virginica were exposed to control or OA conditions, then offspring generated from these adults were exposed to either control or OA conditions. From this experiment, offspring growth rate decreased when offspring were exposed to OA. This effect was partially offset when parents were also exposed to OA, which resulted in an increase in offspring growth rate in exposed conditions relative to offspring from control parents (i.e., transgenerational plasticity). With the animal model I investigated whether different genetic and non-genetic sources of variation could explain variance in larval growth rate from this experiment, including variation due to transgenerational plasticity. In particular, non-genetic sources of variation were represented by measures of parent-specific DNA methylation. I found that both paternal and maternal DNA methylation explained a substantial amount of variation in larval growth rate, with maternal DNA methylation explaining the largest amount of variation. I also found that OA-sensitive DNA methylation (i.e., regions of the methylome differentially methylated in response to OA in parental gametes) explained a significant amount of variation in larval growth rate, indicating that DNA methylation induced in parents may have a role in the transgenerational plasticity we observed in larval growth rate in response to OA. In chapter three, I constructed a quantitative transgenerational plasticity model to investigate the role of environmental predictability and migration on the evolution of transgenerational plasticity. From this model I found that, in general, high parental environment predictability and low or moderate migration most often resulted in the evolution of transgenerational plasticity. However, the magnitude of transgenerational plasticity compared to within-generation plasticity also depended on developmental environment predictability. Under moderate selection strength I observed that the evolution of transgenerational plasticity in combination with within-generation plasticity tended to reduce the genetic variation maintained within a population at evolutionary equilibrium, indicating that the evolution of transgenerational plasticity may limit a population's ability to rapidly evolve via standing genetic variation. Collectively, this work contributes to a growing understanding of the causes and consequences of plasticity under global climate change by providing insight into the molecular mechanism that may mediate plasticity, the environmental and demographic conditions that may result in its evolution, and the implications of evolving transgenerational plasticity on the evolutionary potential of a trait.--Author's abstract