Differentiation in shell traits, mitochondrial coi sequences, and mantle transcriptomes between cultured and wild local populations of Mytilus coruscus in an intensive aquaculture area: A comparison from local to regional scale reveals germplasm homogenization

Large-scale aquaculture poses risks that include genetic and phenotypic homogenization to adjacent wild populations. When comparisons are restricted to areas already impacted by farming, the full extent of these morphological alterations is often obscured. To address this, we conducted a cross-scale analysis to reveal phenotypic trends and their underlying molecular mechanisms in the thick-shelled mussel ( Mytilus coruscus ) from the Ma'an Archipelago, East China Sea. We integrated morphometric measurements, shell mechanics, mitochondrial coi sequencing, and mantle transcriptomics across three distinct groups: aquaculture population (AP), reef-dwelling population near aquaculture zones (RDP), and wild reef-dwelling population distant from aquaculture zones (WRDP). Results revealed a significant phenotypic gradient: AP shells were elongated, thin, and brittle, whereas WRDP shells were robust, exhibiting superior thickness and mechanical strength. Notably, RDP displayed intermediate traits. While coi analysis indicated high genetic connectivity and a lack of significant population structure across the region—suggesting substantial historical gene flow—weighted gene co-expression network analysis (WGCNA) revealed a strong association between phenotype and gene expression. Specifically, cultured mussels exhibited up-regulation of endoplasmic reticulum (ER) stress pathways, suggesting an energy trade-off in which physiological stress responses compromise biomineralization capacity. Consequently, the phenotypic convergence of RDP toward AP highlights a latent risk of germplasm homogenization, even when currently masked by phenotypic plasticity. Our findings strongly suggest that aquaculture activities are reshaping the shell phenotypes of surrounding wild populations, underscoring the urgent need to establish conservation zones that protect offshore wild populations as irreplaceable reservoirs of adaptive potential.