Environmentally-induced DNA methylation is inherited across generations in an aquatic keystone species (Daphnia magna)

Abstract

Environmental stress can result in epigenetic modifications that are passed down several generations. Such epigenetic inheritance can have significant impact on eco-evolutionary dynamics, but the phenomenon remains controversial in ecological model systems. Here, we used whole-genome bisulfite sequencing on individual water fleas (Daphnia magna) to assess whether environmentally-induced DNA methylation can persist for up to four generations. Genetically identical females were exposed to a control treatment, one of three natural stressors (high temperature, zinc, microcystin), or the methylation-inhibitor 5-azacytidine. After exposure, lines were propagated clonally for four generations under control conditions. We identified between 70 and 225 differentially methylated CpG positions (DMPs) between controls and F1 individuals whose mothers (and therefore they themselves as germ cells) were exposed to one of the three natural stressors. Between 46% and 58% of these environmentally-induced DMPs persisted until generation F4 without attenuation in their magnitude of differential methylation. DMPs were enriched in exons and largely stressor-specific, suggesting a possible role in environment-dependent gene regulation. In contrast, treatment with the compound 5-azacytidine demonstrated that pervasive hypo-methylation upon exposure is reset almost completely after a single generation. These results suggest that environmentally-induced DNA methylation is non-random and stably inherited across generations in Daphnia, making epigenetic inheritance a putative factor in the eco-evolutionary dynamics of fresh-water communities.Author summaryWater fleas are important keystone species mediating eco-evolutionary dynamics in lakes and ponds. It is currently an open question in how far epigenetic inheritance contributes to the ability of Daphnia populations to adapt to environmental stress. Using a range of naturally occurring stressors and a multi-generational design, we show that environmentally-induced DNA methylation variants are stably inherited for at least four generations in Daphnia magna. The induced variation in DNA methylation are stressor-specific and almost exclusively found in exons, bearing the signatures of functional adaptations. Our findings imply that ecological adaptations of Daphnia to seasonal fluctuations can be underpinned by epigenetic inheritance of DNA methylation without changes in gene frequencies.

Epigenetic induction may speed up or slow down speciation with gene flow

“…Whether these patterns are due to within-generation plastic responses associated with epigenetic changes or transgenerational inheritance of epigenetic factors, however, is often unclear, but compelling examples exist. In Polygonum plants, drought conditions led parents to produce offspring with longer roots, an adaptive phenotype that has been shown to be mediated by methylation (Herman & Sultan 2016); in stickleback fish, populations from marine environments with different salinities exhibit differences in methylation markers and laboratory experiments that vary salinity have shown that a subset of these same methylation differences are inducible and exhibit transgenerational plasticity, suggesting a role of adaptively inducible epigenetic variation in nature (Heckwolf et al 2020); in Daphnia, stress-induced epigenetic modifications occurred and persisted up to four generations, with modification occurring especially in stress-related genes, suggesting a possible role of heritable epigenetic change in adaptation (Feiner et al 2021).…”

“…2020); in Daphnia , stress‐induced epigenetic modifications occurred and persisted up to four generations, with modification occurring especially in stress‐related genes, suggesting a possible role of heritable epigenetic change in adaptation (Feiner et al. 2021).…”

Epigenetic ecotypes in animals: persistent environmental adaptation in the absence of genetic variation

“…Theoretically, the environmental adaptation of the clonal animals described above and the establishment of epigenetic ecotypes could result from the repeated de novo production of identical, environmentally-induced phenotypes in each generation and/or the transgenerational inheritance and selection of adaptive epigenotypes. The example of the brain coral and recent reviews on the inheritance of epigenotypes (Jablonka, 2017;Anastasiadi et al, 2021;Feiner, 2021;Skinner & Nilsson, 2021) suggest that transgenerational epigenetic inheritance can play an important role in long-term adaptation of genetically uniform populations to different environments, indeed. Final answering of this question requires cross-transplantation experiments and monitoring of epigenetic fingerprints for dozens of generations, which have not been done as yet.…”