Transcriptomic and Metabolomic Insights into Growth Heterosis of Crassostrea hongkongensis Hybrids.

Crassostrea hongkongensis is an economically important mariculture species in southern China, and hybrid breeding has been applied to improve its growth traits. However, the molecular mechanisms underlying growth heterosis remain poorly understood. In this study, inter-population hybrid (HG) and intra-population (IG) groups of C. hongkongensis were compared using integrated transcriptomic and metabolomic analyses to investigate the regulatory basis of growth heterosis. Shell length and shell height were significantly greater in HG than in IG (p < 0.01). Transcriptomic analysis identified 474 false discovery rate (FDR)-supported significant differentially expressed genes (DEGs) (233 upregulated and 241 downregulated), which were treated as the primary statistically robust findings; a broader set of 3161 candidate DEGs, including genes associated with growth regulation and shell biomineralization, was retained for exploratory functional and multi-omics analyses. Metabolomic analysis detected 345 differential metabolites (DMs), which were mainly enriched in energy metabolism, nucleotide metabolism, and arachidonic acid metabolism. Exploratory pathway-level multi-omics integration revealed significant concordance between the transcriptomic and metabolomic profiles (M2 = 0.1962, p = 0.001) and highlighted the tricarboxylic acid cycle, oxidative phosphorylation, branched-chain amino acid degradation, nucleotide metabolism, and arachidonic acid metabolism. These findings suggest that growth heterosis in C. hongkongensis is associated with altered energy metabolism, biosynthetic processes, shell formation-related pathways, and potential changes in the growth-defense balance, providing molecular insights for genetic improvement and selective breeding.