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

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 xenobiotic-induced
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.