Transgenerational effects of intertidal environment on physiological phenotypes and DNA methylation in Pacific oysters

Climate change and intensifying human activity are posing serious threats to marine organisms. The fluctuating intertidal zone forms a miniature ecosystem of a rapidly changing environment for studying biological adaptation. Transgenerational plasticity (TGP), an evolutionary phenomenon in which parental experience influences offspring phenotypes, provides an avenue for adaptation, but the molecular mechanism was poorly understood in marine molluscs. In this study, wild Pacific oysters (Crassostrea gigas), which were collected from intertidal zones, were used to conduct two-generation breeding in a subtidal area combined with a heat shock experiment in the laboratory to investigate the intertidal environment-induced TGP under temperate subtidal condition and thermally exposed condition, respectively. We showed that TGP could influence the physiological phenotypes related to the status of oxidation and energy in non-stress-exposed subtidal offspring for at least two generations. Genomic DNA methylation exhibited heritable divergence between intertidal and subtidal oysters, and 1655 (or 42.83 %) differentially methylated genes (DMGs) in F0 were continuously reserved to F2, which may mediate physiological TGP by participating in biological processes including macromolecule metabolism, cellular responses to stress, and the positive regulation of molecular function, especially fatty acid metabolism. The intertidal experience also influenced the thermal plasticity of physiological phenotypes within and across generations. Totally, 320 (or 14.74 %) specific thermal response DMGs in the intertidal F0 generation were identified in F1 and F2, participating in pathways including carbohydrate, lipid, and energy metabolism, signal transduction, and the organismal immune system, which suggested transgenerational intertidal effect mediated by these genes could positively contribute to stress adaptation and had potential applications for aquaculture. This study demonstrates an epigenetic mechanism for TGP in stress adaptation in marine molluscs, and provides new avenues to improve the stress adaptation for marine resource conservation and aquaculture.