The epigenetics of adaptation: focusing on epigenetic stability as an evolving trait.

“Epigenetics” refers to changes in gene expression that occur through changes in DNA methylation, histone modification, small or micro-RNAs, or most inclusively, other mechanisms that alter how DNA sequences are translated into functional gene products. With the discovery that epigenetic modifications to gene expression can be inherited across cell lineages or even across organismal generations, enormous interest has been generated in the potential evolutionary consequences of epigenetic inheritance. This collection of articles addresses how epigenetic inheritance may influence adaptive evolution, focusing on epigenetic stability and inheritance itself as a potentially evolving trait. It has frequently been argued that epigenetic modifications that are stable across multiple generations can act as an important source of heritable phenotypic variation upon which natural selection can act, and that such variation, unlike random genetic mutation, may even be nonrandom with respect to environmental context and adaptive value. This bold hypothesis raises a number of compelling questions. First, when changes in gene expression are not caused by changes in DNA sequence, what sort of epigenetic changes are stochastic versus environmentally induced, and do they differ in their stability of inheritance? Second, what is the adaptive value of such random and environmentally induced epigenetic modifications in the wild? Third, is the stability of epigenetic alterations itself heritable and is it adaptive, and if so, under what conditions? Does natural selection actually favor epigenetic stability, or not, and does selection for or against stability determine how frequently we may observe adaptation via epigenetic inheritance? These articles begin to address these questions by reviewing recent advances in studies of epigenetics in natural populations. To start, Turck and Coupland explain the molecular basis of two major mechanisms of epigenetic regulation of gene expression: DNA methylation and histone modification. By reviewing case studies in plants, they argue that these two modes of epigenetic regulation can differ in stability and environmental sensitivity. DNA methylation has the potential to be mitotically and meiotically stable, and methylation states can even be passed to homologous alleles or orthologous genes in a genome. Histone modification, in contrast, is involved with environmentally induced epigenetic regulation that can be reversible. Using a case study, the authors show that interspecific differences in the reversibility of environmentally induced gene repression via histone modification are associated with the difference between annual and perennial life histories, and thus likely to have significant adaptive consequences. The authors also hypothesize that the degree of DNA methylation and the stability of environmentally induced changes in gene expression via histone modification may both be associated with changes in the DNA sequence, whether through transposon insertions, tandem duplications, or DNA sequence variation in promoter regions. Such alterations to DNA can cause heritable variation in epigenetic regulation, and thereby be the basis of the evolution of such regulation. Although Turck and Coupland show that differences in DNA methylation and stability of histone modifications can lead to distinct changes in plant life histories, Herman et al. directly address the adaptive value of epigenetic stability by reviewing theoretical