Ancestors’ Gift: Parental Early Exposure to the Environmentally Realistic Pesticide Mixture Drives Offspring Phenotype in a Larger Extent Than Direct Exposure in the Pacific Oyster, Crassostrea gigas

Abstract

Marine organisms are threatened by the presence of pesticides in coastal waters. Among them, the Pacific oyster is one of the most studied invertebrates in marine ecotoxicology where numerous studies highlighted the multiscale impacts of pesticides. In the past few years, a growing body of literature has reported the epigenetic outcomes of xenobiotics. Because DNA methylation is an epigenetic mark implicated in organism development and is meiotically heritable, it raises the question of the multigenerational implications of xenobioticinduced epigenetic alterations. Therefore, we performed a multigenerational exposure to an environmentally relevant mixture of 18 pesticides (nominal sum concentration: 2.85 μg•L −1 ) during embryo−larval stages (0−48 hpf) of a second generation (F1) for which parents where already exposed or not in F0. Gene expression, DNA methylation, and physiological end points were assessed throughout the life cycle of individuals. Overall, the multigenerational effect has a greater influence on the phenotype than the exposure itself. Thus, multigenerational phenotypic effects were observed: individuals descending from exposed parents exhibited lower epinephrine-induced metamorphosis and field survival rates. At the molecular level, RNA-seq and Methyl-seq data analyses performed in gastrula embryos and metamorphosis-competent pediveliger (MCP) larvae revealed a clear F0 treatment-dependent discrimination. Some genes implicated into shell secretion and immunity exhibited F1:F0 treatment interaction patterns (e.g., Calm and Myd88). Those results suggest that low chronic environmental pesticide contamination can alter organisms beyond the individual scale level and have long-term adaptive implications.

DNA methylation correlates with transcriptional noise in response to elevated pCO2in the eastern oyster (Crassostrea virginica)

“…Following mammalian studies, it was previously considered that environmentally-sensitive changes in methylation drive differential expressed genes on a gene-by-gene basis in marine invertebrates. However, to date, numerous molluscan studies have failed to find any significant relationships between differential DNA methylation and differential gene expression [36,39,444], or have found minimal overlaps in differentially expressed genes and differentially methylated regions [43,54]. As described above, we could not examine the association between differential methylation and differential gene expression since we did not observe any of the latter.…”