Abstract
Genetic responses of oysters to specific environments underpin adaptation and evolutionary potential, which can be leveraged through breeding to improve outcomes. Shell traits strongly influence both survival and market value in the half-shell market. Using novel trait phenotyping methods, the heritability, genetics-by-environment interactions, and potential surrogate traits for shell integrity (hardness, chalkiness, density, compressive strength) and other market-preferred phenotypes were investigated in twenty full-sib pedigree-bred Pacific oyster family lines. Of twenty traits assessed, shell colour had the highest heritability ([Formula: see text] = 0.93, 0.78, in faster- and slower-growth estuaries respectively). Shell integrity traits exhibited moderate heritabilities ([Formula: see text]=0.12–0.40), growth traits had low to moderate heritabilities ([Formula: see text] = 0.08– 0.26), and meat yield/condition had values near zero. Higher trait heritabilities were identified for many morphometric and somatic metrics, as well as meat yield phenotypes, in the slower-growth estuary. The faster-growth estuary had higher heritabilities for shell colour and density. Phenotypic expression under reduced growth aligned with industry-favourable shell qualities, including denser, darker, less brittle shells with deeper cups, whereas fast growth produced diminished shell integrity but with superior meat yield. Genetic correlations indicate that selection on readily measurable whole, shell and meat weight traits, alongside colour, could improve shell integrity, reduce production losses and enable farmers to consistently deliver better-quality oysters to market. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1038/s41598-025-34267-x.