Pollution induces epigenetic effects that are stably transmitted across multiple generations

Abstract

It has been hypothesized that the effects of pollutants on phenotypes can be passed to subsequent generations through epigenetic inheritance, affecting populations long after the removal of a pollutant. But there is still little evidence that pollutants can induce persistent epigenetic effects in animals. Here, we show that low doses of commonly used pollutants induce genome‐wide differences in cytosine methylation in the freshwater crustacean Daphnia pulex. Uniclonal populations were either continually exposed to pollutants or switched to clean water, and methylation was compared to control populations that did not experience pollutant exposure. Although some direct changes to methylation were only present in the continually exposed populations, others were present in both the continually exposed and switched to clean water treatments, suggesting that these modifications had persisted for 7 months (>15 generations). We also identified modifications that were only present in the populations that had switched to clean water, indicating a long‐term legacy of pollutant exposure distinct from the persistent effects. Pollutant‐induced differential methylation tended to occur at sites that were highly methylated in controls. Modifications that were observed in both continually and switched treatments were highly methylated in controls and showed reduced methylation in the treatments. On the other hand, modifications found just in the switched treatment tended to have lower levels of methylation in the controls and showed increase methylation in the switched treatment. In a second experiment, we confirmed that sublethal doses of the same pollutants generate effects on life histories for at least three generations following the removal of the pollutant. Our results demonstrate that even low doses of pollutants can induce transgenerational epigenetic effects that are stably transmitted over many generations. Persistent effects are likely to influence phenotypic development, which could contribute to the rapid adaptation, or extinction, of populations confronted by anthropogenic stressors.

Adapting to climate with limited genetic diversity: Nucleotide,DNAmethylation and microbiome variation among populations of the social spiderStegodyphus dumicola

“…This implies that only a subset of methylation variants may differentiate among populations. DNA methylations can be induced by environmental variance as shown in fish, mammals, plants, birds and invertebrates (Bossdorf et al, 2008 ; Cropley et al, 2012 ; Harney et al, 2022 ; Heckwolf et al, 2019 ; Nätt et al, 2012 ), and are proposed to have the potential to modulate phenotypes in a plastic manner (Duncan et al, 2022 ; Flores et al, 2012 ; Gatzmann et al, 2018 ; Marshall et al, 2019 ). Furthermore, inducible DNA methylations can be transmitted across generations, which exposes them to evolutionary forces at least on short timescales (Cubas et al, 1999 ; Nätt et al, 2012 ; Riddle & Richards, 2002 ; Sutherland et al, 2000 ).…”

“…This is consistent with the idea that variation in phenotypes may be mediated by environmentally induced changes in DNA methylation profiles, which may facilitate the ability of populations to cope with changes in local climatic conditions on a shorter timescale than that of adaptive genetic changes. Furthermore, studies have shown that epigenetic changes can be heritable and may persist across generations (Harney et al, 2022 ; Nätt et al, 2012 ; Riddle & Richards, 2002 ; Sutherland et al, 2000 ). Studies on how DNA methylation variation is structured across geographical locations and combining this with variation in environmental factors such as, for example, temperature and precipitation, can inform and substantiate hypotheses on the role of DNA methylation in generating locally advantageous phenotypes.…”

Caste- and sex-specific DNA methylation in a bumblebee is associated with codon degeneracy

“…As discussed in Dixon and Matz (2022), gene-body DNA methylation does not appear to directly regulate gene expression in invertebrates. However, recent papers have suggested a role for DNA methylation in species evolution, whereby environmentally induced DNA methylation is directly heritable (Skinner and Nilsson, 2021; Harney et al ., 2022) and may produce adaptive phenotypes. Multiple studies in arthropods have indeed demonstrated heritability of DNA methylation (e.g.…”

“…Multiple studies in arthropods have indeed demonstrated heritability of DNA methylation (e.g. Wang et al ., 2016; Yagound et al ., 2020) including environmentally induced DNA methylation (Harney et al ., 2022). Given that DNA methylation has also been shown to be linked to the underlying genotype in various insect species (Wang et al ., 2016; Marshall et al ., 2019; Yagound et al ., 2019, 2020; Wu et al ., 2020) we predicted that it may be enriched in certain codon positions in order to provide substrate for selection, not through directly altering gene expression levels but through its mutagenic effect on the underlying genome, which may then cause transcriptional variation.…”

Environmental Adaptation of Genetically Uniform Organisms with the Help of Epigenetic Mechanisms—An Insightful Perspective on Ecoepigenetics

“…However, most studies in animals and plants were run for 1–3 generations only [ 179 ]. Exceptions include some studies with water flea Daphnia pulex , nematode Caenorhabditis elegans , tale cress Arabidopsis thaliana and the unicellular green alga Chlamydomonas reinhardtii , which were run for 15, >20, 30 and ~200 generations, respectively [ 180 , 181 , 182 , 183 ]. New studies over many more generations are necessary to obtain a better picture.…”