While environmentally inducible epigenetic marks are discussed as one mechanism of transgenerational plasticity, environmentally stable epigenetic marks emerge randomly. When resulting in variable phenotypes, stable marks can be targets of natural selection analogous to DNA sequence-based adaptation processes. We studied both postulated pathways in natural populations of three-spined sticklebacks (Gasterosteus aculeatus) and sequenced their methylomes and genomes across a salinity cline. Consistent with local adaptation, populations showed differential methylation (pop-DMS) at genes enriched for osmoregulatory processes. In a two-generation experiment, 62% of these pop-DMS were insensitive to salinity manipulation, suggesting that they could be stable targets for natural selection. Two-thirds of the remaining inducible pop-DMS became more similar to patterns detected in wild populations from the corresponding salinity, and this pattern accentuated over consecutive generations, indicating a mechanism of adaptive transgenerational plasticity. Natural DNA methylation patterns can thus be attributed to two epigenetic pathways underlying the rapid emergence of adaptive phenotypes in the face of environmental change.

Supplement to: Heckwolf, Melanie; Meyer, Britta S; Häsler, Robert; Höppner, Marc P; Eizaguirre, Christophe; Reusch, Thorsten B H (2020): Two different epigenetic information channels in wild three-spined sticklebacks are involved in salinity adaptation. Science Advances, 6(12), eaaz1138