Ecological divergence of DNA methylation patterns at distinct spatial scales

Adaptive trait divergence between populations is regulated by genetic and non-genetic processes. Compared to genetic change, epigenetic change is unstable and short-lived, questioning its contribution to long-term adaptive potential. However, epigenetic change can accumulate over time, and may result in beneficial epigenetic memories where environments are heterogeneous. Diverging epigenetic memories have been observed across large spatial scales, and can persist through multiple generations even in the absence of the causative environmental stressor. It is unknown, however, how and to what extent epigenetic memories contribute to fine-scale population structure and evolution. Here, we performed whole genome bisulfite sequencing on 30 Fragaria vesca F1 plants originating from distinct ecological settings and grown in a controlled environment. Specifically, we compared methylation patterns between a steep, altitudinal gradient (<2 km) and a wide spatial gradient (>500 km). If epigenetic variation is random, arising from errors during replication and without evolutionary implications, one would expect similar amounts of epigenetic variation across populations and no spatial scale-effect. Here, we find that epigenetic memories arise even at fine spatial scale, and that both parallel and non-parallel biological processes underpin epigenetic divergence at distinct spatial scales. For example, demethylation of transposable elements consistently occurred at the large but not the small spatial scale, while methylation differentiation for most biological processes were shared between spatial scales. Acute drought stress did not result in significant epigenetic differentiation, indicating that repeated historical stress levels associated with heterogeneous environmental conditions are required for acquiring a stable epigenetic memory and for coping with future environmental change.