Evidence for epigenetically influenced mutagenesis and genetic assimilation in nascent species complexes (Coregonussp.)

Abstract

AbstractPhenotypic diversification and speciation are classically associated with genetic differentiation and gene expression variation. However, increasing evidence suggests that epigenetic mechanisms like DNA methylation may contribute to species divergence due to their effects on transcription and phenotype. Methylation can also increase mutagenesis and could lead to genetic assimilation of plastic phenotypes into genetic variants when the environment remains stable over many generations, though there has been minimal empirical research on assimilation. Whitefish are excellent systems to study speciation and genetic assimilation due to the repeated independent divergence of benthic-limnetic species pairs that have coexisted in lakes for ~12 000 years serving as natural replicates. Here we investigate whole genome genetic and epigenetic differentiation between benthic-limnetic species pairs in lake whitefish (Coregonus clupeaformis) and European whitefish (C. lavaretus) from four lakes (N=64). We found considerable, albeit variable, genetic and epigenetic differences between benthic and limnetic species in all four lakes. Polymorphism was enriched at CpG sites confirming the mutagenic nature of DNA methylation; all SNP types were enriched in all lakes, though C > T SNPs were most common. We also identified a surplus of potential sites undergoing genetic assimilation putatively associated with speciation, defined as sites harbouring both a differentially methylated site and a highly divergent SNP. Our results support the hypothesis that DNA methylation contributes to phenotypic divergence, influences mutagenesis, and drives genetic assimilation of phenotypes that are ultimately associated with ecological speciation in whitefish species complexes.