Fishing pressure induces changes in DNA methylation in genetically homogeneous marine metapopulations

Trait-selective harvesting by fisheries can impose strong selective pressures on fish populations, driving changes in life history traits affecting fisheries productivity and ecosystem functioning. While the genetic consequences of harvesting have been extensively studied, the extent to which phenotypic variation reflects genomic evolution versus environmentally-induced plasticity remains unclear. Epigenetic mechanisms, such as DNA methylation, may mediate between these processes, serving as a rapid and reversible response to the selective pressures imposed by harvesting. In this study, we implemented an improved laboratory and bioinformatics protocol, epiGBS3, to examine genomic variation and DNA methylation patterns in the marine fish Xyrichtys novacula. The study spanned three replicated geographical areas each comprising two adjacent locations: an intensively exploited fishery and a no-take Marine Protected Area (ntMPA). A nested analysis design across the three areas revealed strong gene flow and no evidence of genetic structure. Nevertheless, nucleotide diversity was significantly reduced in fisheries relative to ntMPAs. We also found that DNA methylation levels differed between protected and exploited sites after controlling for age, suggesting that fishing may influence epigenetic changes independently of fisheries-induced age-truncation effects. This represents one of the first lines of evidence that fisheries can potentially shape epigenetic variation, supporting DNA methylation as contributor to local adaptation under high gene flow and strong anthropogenic selection.