Decoupled genetic and epigenetic variation in the montane endemic Erodium cazorlanum (Geraniaceae) and a widespread congener

Abstract

Epigenetic states offer an additional layer of variation besides genetic polymorphism that contribute to phenotypic variation and may arise either randomly or in response to environmental factors. We hypothesize that closely related species with different life-histories and habitat requirements could show distinct patterns of intraspecific epigenetic variation. We used Restriction-site Associated DNA sequencing (RADseq) and its bisulfite-converted variant (bsRADseq) to investigate in Sierra de Cazorla (SE Spain) the genetic and epigenetic population structure of two congeneric species, the endemic woody perennial Erodium cazorlanum and the widely distributed annual herb E. cicutarium. Population genomics analyses revealed no structure in either E. cazorlanum and E. cicutarium, suggesting substantial gene flow between the study populations. In contrast, we found that the mean proportion of global DNA methylation was different between populations and species, with E. cazorlanum DNA showing higher methylation average and across-individuals variation. For each species, we searched for the loci with the strongest epigenetic differentiation between populations (differentially methylated cytosines, DMCs), and summarized them across regions (differentially methylated regions, DMRs). Multivariate analysis and hierarchical clustering of single cytosines methylation percentages did not group individuals by population, pointing to high epigenetic variation within populations. DMRs were enriched in Copia transposable elements, putatively associated with stress response in plants. Our results suggest that variation at both genetic and epigenetic levels in our study area occur mainly within natural populations of E. cazorlanum and E. cicutarium, with stronger population structure in E. cicutarium, and highlight the relevance of analyzing short distance spatial patterns.