The role of stochasticity in the origin of epigenetic variation in animal populations

Epigenetic mechanisms such as DNA methylation modulate gene expression in a complex fashion are consequently recognized as among the most important contributors to phenotypic variation in natural populations of plants, animals, and microorganisms. Interactions between genetics and epigenetics are multifaceted and epigenetic variation stands at the crossroad between genetic and environmental variance, which make these mechanisms prominent in the processes of adaptive evolution. DNA methylation patterns depend on the genotype and can be reshaped by environmental conditions, while transgenerational epigenetic inheritance has been reported in various species. On the other hand, DNA methylation can influence the genetic mutation rate and directly affect the evolutionary potential of a population. The origin of epigenetic variance can be attributed to genetic, environmental, or stochastic factors. Generally less investigated than the first two components, variation lacking any predictable order is nevertheless present in natural populations and stochastic epigenetic variation, also referred to spontaneous epimutations, can sustain phenotypic diversity. Here, potential sources of such stochastic epigenetic variability in animals are explored, with a focus on DNA methylation. To this day, quantifying the importance of stochasticity in epigenetic variability remains a challenge. However, comparisons between the mutation and the epimutation rates showed a high level of the latter, suggesting a significant role of spontaneous epimutations in adaptation. The implications of stochastic epigenetic variability are multifold: by affecting development and subsequently phenotype, random changes in epigenetic marks may provide additional phenotypic diversity, which can help natural populations when facing fluctuating environments. In isogenic lineages and asexually reproducing organisms, poor or absent genetic diversity can hence be tolerated. Further implication of stochastic epigenetic variability in adaptation is found in bottlenecked invasive species populations and populations using a bet-hedging strategy.