A Comprehensive Analysis of Transcriptomics and Proteomics Elucidates the Cold-Adaptive Ovarian Development of Eriocheir sinensis Farmed in High-Altitude Karst Landform

Background: In high-altitude regions, sporadic two-year-old immature Chinese mitten crabs (Eriocheir sinensis) would overwinter and mature in their third year, developing into three-year-old crabs (THCs) with a cold-adaptive strategy. Compared to two-year-old crabs (TWCs) from low-altitude Jiangsu, THCs from Karst landform and high-altitude Guizhou exhibit significantly larger final size but lower gonadosomatic index (GSI) (p < 0.01). Methods: To elucidate the molecular mechanisms underlying this delayed ovarian development, integrated transcriptomic and proteomic analyses were conducted. Results: Results showed downregulation of PI3K-Akt and FoxO signaling pathways, as well as upregulation of protein digestion and absorption pathways. Differentially expressed proteins indicated alterations in mitochondrial energy transduction and nutrient assimilation. Integrated omics analysis revealed significant changes in nucleic acid metabolism, proteostasis, and stress response, indicating systemic reorganization in energy-nutrient coordination and developmental plasticity. Conclusions: The observed growth-reproductive inverse relationship reflects an adaptive life-history trade-off under chronic cold stress, whereby energy repartitioning prioritizes somatic growth over gonadal investment. Our transcriptomic and proteomic data further suggest a pivotal regulatory role for FOXO3 dephosphorylation in potentially coupling altered energy sensing to reproductive suppression. This inferred mechanism reveals a potential conserved pathway for environmental adaptation in crustaceans, warranting further functional validation.