DNA methylation facilitates local adaptation and adaptive transgenerational plasticity

Epigenetic inheritance has been suggested to contribute to adaptation via two distinct pathways. Either, stable epigenetic marks emerge as epimutations and are targets of natural selection via the phenotype, analogous to adaptation from DNA sequence-based variation. Alternatively, epigenetic marks are inducible by environmental cues, possibly representing one mechanism of transgenerational phenotypic plasticity. We investigated whether both postulated pathways are detectable in nature and sequenced methylomes and genomes of three-spined sticklebacks (Gasterosteus aculeatus) across a natural salinity gradient in a space-for-time approach. Consistent with local adaptation patterns, stickleback populations showed differentially methylated CpG sites (pop-DMS) at genes enriched for osmoregulatory processes. In a two-generation salinity acclimation experiment with fish from the mid salinity, we found the majority (62%) of pop-DMS to be insensitive to experimental salinity change, suggesting that they were shaped by selection and facilitate local salinity adaptation. Among the experimentally inducible DMS, two-thirds increased in similarity to anticipated adaptive patterns in wild populations under exposure to the novel salinity. This study demonstrates the presence of two types of methylation marks, inducible and stable, that contribute to adaptive transgenerational plasticity and local adaptation in natural populations.