4.5 Article

Pollution induces epigenetic effects that are stably transmitted across multiple generations

Journal

EVOLUTION LETTERS
Volume 6, Issue 2, Pages 118-135

Publisher

OXFORD UNIV PRESS
DOI: 10.1002/evl3.273

Keywords

Cytosine methylation; Daphnia pulex; ecotoxicology; gene body methylation; transgenerational epigenetic inheritance

Funding

  1. Natural Environment Research Council, UK [NE/I024437/1, NE/N016017/1]
  2. NERC [NE/N016017/1, NE/I024437/1] Funding Source: UKRI

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This study demonstrates that low doses of pollutants can induce transgenerational epigenetic effects in freshwater crustaceans, affecting the methylation patterns of the genome. These effects can persist for multiple generations and can be inherited even after the removal of the pollutant. The altered methylation levels may lead to phenotypic changes and potentially contribute to the adaptation or extinction of populations facing anthropogenic stressors.
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.

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