Growth Variation in the Pacific Oyster (Crassostrea gigas) Is Associated with Sequential Transcriptional Programs of Tissue Differentiation

Growth variation is one of the most economically important traits in oyster aquaculture, yet the transcriptional programs associated with divergent growth performance remain incompletely understood. In this study, three growth cohorts of the Pacific oyster (Crassostrea gigas) originating from the same production batch were examined to characterize coordinated differences in tissue-associated transcriptional programs across contrasting growth cohorts. A total of 25 RNA-seq libraries were generated from slow-growth (SG) whole-body samples and mantle and gill tissues of medium-growth (MG) and fast-growth (FG) oysters. RNA-seq analysis identified 28,773 expressed genes and 9373 differentially expressed genes (|log2FC| ≥ 2, FDR ≤ 0.05). Tissue-specific analysis further identified 1407 mantle-specific and 773 gill-specific genes, reflecting distinct functional specialization of the two tissues. Weighted gene co-expression network analysis (WGCNA) resolved six biologically interpretable modules associated with growth state and tissue identity. When module eigengene patterns were examined across the ordered SG–MG–FG continuum, the modules showed sequential shifts from SG-associated basal metabolic and RNA-processing programs to MG-associated tissue-specialization programs and FG-associated mature mantle and gill functional programs. The FG mantle-associated module was enriched for chitin remodeling, shell matrix-related functions, and structural organization, whereas the FG gill-associated module showed enrichment of Toll-like receptor signaling, epithelial organization, and innate immune functions. Expression patterns of representative genes from the six modules were independently validated by quantitative RT-PCR and showed strong concordance with the RNA-seq data. Collectively, these results identify coordinated differences in basal and tissue-associated transcriptional programs across contrasting growth cohorts. This framework provides a transcriptomic basis for interpreting growth-associated tissue maturation and identifies candidate molecular indicators for future validation in oyster selective breeding.