Abstract
Epigenetic components are hypothesized to be sensitive to the environment, which should permit species to adapt to environmental changes. In wild populations, epigenetic variation should therefore be mainly driven by environmental variation. Here, we tested whether epigenetic variation (DNA methylation) observed in wild populations is related to their genetic background, and/or to the local environment. Focusing on two sympatric freshwater fish species (Gobio occitaniae and Phoxinus phoxinus), we tested the relationships between epigenetic differentiation, genetic differentiation (using microsatellite and single nucleotide polymorphism (SNP) markers), and environmental distances between sites. We identify positive relationships between pairwise genetic and epigenetic distances in both species. Moreover, epigenetic marks better discriminated populations than genetic markers, especially in G. occitaniae. In G. occitaniae, both pairwise epigenetic and genetic distances were significantly associated to environmental distances between sites. Nonetheless, when controlling for genetic differentiation, the link between epigenetic differentiation and environmental distances was not significant anymore, indicating a noncausal relationship. Our results suggest that fish epigenetic variation is mainly genetically determined and that the environment weakly contributed to epigenetic variation. We advocate the need to control for the genetic background of populations when inferring causal links between epigenetic variation and environmental heterogeneity in wild populations.
Highlights
Describing and understanding spatial patterns of intraspecific diversity in natural populations constitutes the basis for predicting the evolutionary dynamics of populations
For G. occitaniae, the part of the total variance explained by the between-population component was twice as high for epigenetic markers as it was for genetic markers (20.15% and 10.34%, respectively, see Table 2)
For P. phoxinus, a similar trend was observed less pronounced (19.59% and 16.75%, respectively, see Table 2). This suggests that, in both species, epigenetic markers were more powerful to discriminate among populations than genetic markers
Summary
Describing and understanding spatial patterns of intraspecific diversity in natural populations constitutes the basis for predicting the evolutionary dynamics of populations. Epigenetic variation may allow for the rapid adaptation of populations to changing environments, at a pace higher than adaptation by natural selection on standing genetic variation [5,8,9,10,11] In this context, an important question concerns the spatial covariation that may exist between genetic and epigenetic diversity patterns in natural populations, i.e., whether genetic and epigenetic variants follow similar spatial patterns across landscapes or not. An important question concerns the spatial covariation that may exist between genetic and epigenetic diversity patterns in natural populations, i.e., whether genetic and epigenetic variants follow similar spatial patterns across landscapes or not Answering this question allows testing whether these two markers carry distinct/complementary pieces of information, and speculating about their relative roles in the adaptive potential of organisms across spatial scales. This question is not trivial, as the inherent characteristics of genetic and epigenetic marks can lead to opposite predictions regarding the spatial covariation of epigenetic and genetic diversity patterns
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