Molecular insights into performance-related heterosis in offspring have been revealed by a hybrid oyster (Crassostrea dianbaiensis ♀ × C. iredalei ♂)

Interspecific hybridization represents a significant approach for developing enhanced economic traits in aquatic species, and it was established in oyster breeding. However, early research has still needed to further deepen the understanding of the mechanisms of oyster hybridization advantages. Prior research has indicated that Crassostrea iredalei and C. dianbaiensis, as locally unique varieties, are used to hybridize and obtain excellent performance progeny, and analytical hybrid advantages may be representative. In this study, hybrid oyster DI (C. dianbaiensis ♀ × C. iredalei ♂) and its parents were subjected to long-term in situ tracking (180-day-old, 270-day-old, and 360-day-old), and comprehensively evaluated the dynamic regulation of physiological indicators and molecular levels related to hybrid dominance. Our findings revealed that hybrid progeny showed excellent performance in both growth and survival rate. In addition, the survival level of the DI population under different salinity stress is higher than that of its parents, which once again proves that DI has excellent phenotypic characteristics of heterosis. Transcriptome results from both tissues also support the gene expression pattern of the offspring approaching maternal genes. This maternal effect shows similar functional classifications in both the adductor muscle and the mantle, mainly reflected in the proliferation, metabolism, and immune resistance of cells, implying that the hybrid advantage of hybrid progeny comes from the main effect of the maternal parent. Simultaneously, genes exhibiting a positive-dominant expression pattern, originating from parental effector genes, have also been identified. Interestingly, candidate genes (ADAMTS16, FUCA1, PI4KA, SLC7A9, TCF7L2, and CSNK2A2) are considered to be markers related to growth traits in other aquatic animals. Candidate genes associated with immunomodulatory signaling pathways and resistance (SMAD4, MYD88, BIRC3, BIRC7, and PPTC7) were also screened. Notably, genes related to salinity adaptive regulation (SLC23A2 and SLC12A1) were screened, suggesting the potential and diversity of molecular regulation of heterosis. In short, hybrid oyster DI has obvious hybrid advantages in growth and stress resistance, POD genes, notably TCF7L2 and SLC12A1, are proposed as selectable markers for high-yield, stress-resilient oyster lines, and our findings provide the necessary theoretical perspective for a deep understanding of the hybrid advantages of oysters and their generation mechanism.