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.

Understanding the evolutionary responses of organisms to thermal regimes is of prime importance to better predict their ability to cope with ongoing climate change. Although this question has attracted interest in free-living organisms, whether or not infectious diseases have evolved heterogeneous responses to climate is still an open question. Here, we ran a common garden experiment using the fish ectoparasiteTracheliastes polycolpus, (i) to test whether parasites living in thermally heterogeneous rivers respond differently to an experimental thermal gradient and (ii) to determine the evolutionary processes (natural selection or genetic drift) underlying these responses. We demonstrated that the reaction norms involving the survival rate of the parasite larvae (i.e. the infective stage) across a temperature gradient significantly varied among six parasite populations. Using aQ_st/F_stapproach and phenotype–environment associations, we further showed that the evolution of survival rate partly depended upon temperature regimes experiencedin situ, and was mostly underlined by diversifying selection, but also—to some extent—by stabilizing selection and genetic drift. This evolutionary response led to population divergences in thermal tolerance across the landscape, which has implications for predicting the effects of future climate change.