Ecological divergence of DNA methylation patterns at distinct spatial scales

Abstract

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.

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

“…Interpretation of the results obtained for the portion of genome here explored should take into account that due to the relatively high GC content in the recognition site of the specific enzyme we used (PstI that cuts at CTGCAG), bsRADseq dataset is enriched for genic regions (Lea et al, 2017;Trucchi et al, 2016) and, thus, quantitative global estimates would be less accurate for genomes with a relative high content of repetitive elements (i.e., in E. cazorlanum according to its larger genome size). Nevertheless, percentages of cytosine methylation per sequence context in the two species were consistent among each other and also with those reported for other plant species with complete methylomes, i.e., CpG higher than CHG, CHH being the lowest (Cokus et al, 2008;De Kort et al, 2020;Hsu et al, 2017;Zhao et al, 2020). The higher proportion of methylated to unmethylated cytosines obtained in E. cazorlanum is consistent with a marked difference in percentages obtained from independent analyses conducted by HPLC to obtain global DNA methylation estimates for the two species (28.4 % vs. 18.2 %; Alonso unpublished data).…”

“…The genomic and ecological features that could be associated to the broad variation in levels of DNA methylation mentioned above are still poorly understood. Particularly for non-model plant species, contrasting evidences have been found regarding their variation across natural populations and geographic-climatic gradients (see e. g. De Kort et al, 2020;Galanti et al, 2022;Lamka et al, 2022;Richards et al, 2017;Richards et al, 2010).…”