Conserved sex-biased DNA methylation patterns target key developmental genes and non-recombining region of the guppy sex chromosome

ABSTRACT Understanding the regulatory mechanisms that control sexually dimorphic gene expression is a key part of understanding the processes that govern the rate of sex chromosome evolution and phenotypic sex differences. Epigenetic modifications play a major role in tissue-specific gene expression regulation and have been hypothesized to dramatically impact the speed of sex chromosome divergence. The guppy sex chromosomes are an emerging model for studying the initial stages of divergence between the X and Y. In this study, we use comparative epigenomics to identify conserved sex-specific DNA methylation patterns in gonad and muscle tissue between the Trinidadian guppy (Poecilia reticulata) and its sister species, Endler’s guppy (Poecilia wingei). We find that the oldest part of the guppy sex chromosome shows a conserved pattern of male hypomethylation, consistent with a key role in testis-specific gene expression. This pattern provides a potential mechanism for theoretical predictions that sex chromosome divergence can occur remarkably quickly in evolutionary time, and without widespread degradation of the Y chromosome gene content. Our cross-species comparative epigenomic analysis also provides a robust comparative framework to understand constraints of epigenetic programming. We observe conserved, testis-specific hypomethylated regions near key autosomal developmental genes and a potentially imprinted locus. These observations are consistent with DNA methylation in testis from other vertebrates, and suggest broad conservation of DNA methylation patterns in these regions. Our comparative framework reveals conserved DNA methylation differences between males and females across two related species, providing novel insights into the relationship between epigenetic and evolutionary processes.