ABSTRACT Repeated adaptive divergence in replicates of phenotypic diversification offers a propitious context to identify the molecular bases associated to adaptive divergence. A currently hotly debated topic pertains to the relative role of genomic vs. epigenomic variation in shaping patterns of phenotypic variation at the gene expression level. Here, we combined genomic, epigenomic and transcriptomic information from 64 individuals in order to quantify the relative role of SNPs and DNA methylation variation in the repeated evolution of four limnetic-benthic whitefish species pairs from Europe and North America. We first found evidence for 149 convergent differentially methylated regions (DMRs) between species across continents, which significantly influenced levels of gene expression. Hyper-methylated DMRs in the limnetic species were globally associated to an expression repression relatively to benthic species, and inversely. Furthermore, we identified 108 convergent genetic variants (eQTLs) associated to gene expression differences between species. Gene expression differences were more pronounced in genes harbouring eQTL compared to those associated with DMRs, thus revealing a greater effect of eQTLs on gene expression. Multivariate analyses allowed partitioning the relative contribution of epi-/genomic changes and their association to gene expression variation. Most of the gene expression variation was significantly explained by genomic (4.1%) and putatively genomic-epigenomic interactive variation (46.7%), while “pure” epigenomic variation explained marginally 2.3% of the gene expression variation across continents. This study provides a rare qualitative and quantitative documentation of the relative role of genomic, DNA methylation and their interaction in shaping patterns of convergent gene expression during the process of ecological speciation.

The role of genomic vs. epigenomic variation in shaping patterns of convergent transcriptomic variation across continents in a young species complex