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Environmental Research
Volume 197, 2021, 111058

Direct and heritable effects of natural tidal environments on DNA methylation in Pacific oysters (Crassostrea gigas)

Xinxing Wanga,c,d, Ao Lia,d,e,f, Wei Wanga,d,e,f, Guofan Zhanga,b,e,f, Li Lia,d,e,f

CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China.

Abstract

Rapid climate change threatens the survival of animals, especially in vulnerable coastal ecosystems. Recent studies have shown that DNA methylation is a mechanism by which organisms can modulate current and future generations to cope with rapid environmental changes. Here, an investigation in a real-world context was conducted to determine the epigenetic mechanisms that are triggered by environmental changes in a typical intertidal species, the Pacific oyster (Crassostrea gigas). Oysters inhabiting intertidal and subtidal regions were collected, and their offspring were produced and subjected to common environment. The divergence of phenotypes and whole genome DNA methylation were assayed between the intertidal and subtidal oysters. The undifferentiated genetic structures implied that the phenotypic and epigenetic variations were mainly induced by the environment. Approximately 41% of genes modified by DNA methylation, which play a role in responses to the variable intertidal environment, could be transmitted to the next generation and had largely consistent tendency of regulation. The cross-generational genes were involved in the regulation of GTPase activity, primary metabolic activity, autophagosomes, and apoptosis, which may mediate the inheritable phenotypic divergence related to heat stress resistance between intertidal and subtidal oysters. The extent to which environmentally induced DNA methylation is inherited was evaluated here for the first time in oysters. This study provides new insights into the epigenetic mechanisms underlying biological adaptations to rapid climate change in coastal organisms.

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