DNA methylation shows footprints of altitude selection in the clonal plant speciesFragaria vesca

Abstract

Climate change poses a significant threat to plant species, potentially pushing them beyond their adaptive capacities. Epigenetic modifications, such as DNA methylation, have emerged as a key candidate mechanism enabling plants to quickly adapt to environmental changes by generating locally adapted phenotypes. These phenotypic changes can be even inherited across multiple generations, thus potentially becoming targets of natural selection. However, whether natural selection can act on these epialleles has hardly been tested directly. Addressing this knowledge gap is crucial as population survival may heavily rely on DNA methylation, especially in scenarios with restricted genetic diversity, such as within clonal plant populations. Here, we employed population genomics approaches on seven natural populations of the clonal species wild strawberry (Fragaria vesca) distributed across an altitudinal range to investigate the presence of epigenetic sites under altitude-driven selection. Our genomic, epigenomic, and transcriptomic analyses found a wide intra- and inter-population epigenetic diversity despite a considerably low genetic diversity. We identified heritable epialleles exhibiting signs of positive selection related to altitude, i.e. reduced intrapopulation epigenetic diversity and increased epigenetic divergence between low and high altitude. These altitude-selected epigenetic loci overlapped with genes involved in biological processes such as DNA repair, molecular recognition, regulation of gene expression, and chromatin structure. Interestingly, some of these epialleles were independent of genetic variation, suggesting they may have arisen stochastically or in response to environmental variation. These findings suggest that heritable epigenetic variation could help clonal species quickly adapt to environmental challenges as those related to varying altitudes and/or temperatures.