ABSTRACT
Epigenetic inheritance can drive adaptive evolution independently of DNA sequence variation. However, to what extent epigenetic variation represents an autonomous evolutionary force remains largely elusive. Through gene ontology and comparative analyses of genomic and epigenomic variation of wild strawberry plants raised in distinct drought settings, we characterised genome-wide covariation between single nucleotide polymorphisms (SNPs) and differentially methylated cytosines (DMCs). Covariation between SNPs and DMCs was independent of genomic proximity, but instead associated with fitness-related processes such as stress responses, genome regulation and reproduction. We expected this functional SNP-DMC covariation to be driven by adaptive evolution canalising SNP and DMC variation, but instead observed significantly lower covariation with DMCs for adaptive rather than for neutral SNPs. Drought-induced DMCs frequently co-varied with tens of SNPs, suggesting high genomic redundancy as a broad potential basis for polygenic adaptation of gene expression. Our findings suggest that stress-responsive DMCs initially co-vary with many SNPs under increased environmental stress, and that natural selection acting upon several of these SNPs subsequently reduces standing covariation with stress-responsive DMCs. Our study supports DNA methylation profiles that represent complex quantitative traits rather than autonomous evolutionary forces. We provide a conceptual framework for polygenic regulation and adaptation shaping genome-wide methylation patterns in plants.