Stage-resolved multi-tissue transcriptomics reveals coordinated molecular responses during feeding in Babylonia...

Feeding is a fundamental physiological process in mollusks and requires coordinated sensory, neural, and metabolic responses across multiple tissues. However, the cross-tissue molecular mechanisms underlying feeding in gastropods remain largely unexplored. In this study, we conducted a multi-tissue comparative transcriptomic analysis of Babylonia areolata across four key feeding stages, including pre-feeding, feeding initiation, satiation, and post-feeding, to characterize dynamic molecular responses in the osphradium, cephalic region, and hepatopancreas. Integrated analyses of differential expression, functional enrichment, and weighted gene co-expression network analysis (WGCNA) were used to reconstruct a cross-tissue regulatory framework. Feeding triggered distinct yet temporally coordinated transcriptional programs across tissues. The osphradium showed rapid activation of neuroactive ligand-receptor interaction, calcium signaling, and Wnt pathways, supporting its role as the primary chemosensory gateway that converts food-derived cues into neural signals. The cephalic region exhibited multi-phasic neuroactive and Wnt signaling responses, corresponding to phases of sensory readiness, neural activation, and post-feeding modulation. In contrast, the hepatopancreas displayed a stage-specific metabolic progression, transitioning from lysosomal digestive activation to enhanced amino acid and nucleotide biosynthesis, followed by lipid remodeling, antioxidant defense, and immune regulation during the post-feeding period. Together, these results reveal a hierarchical "sensing-integration-execution" cascade that links chemosensory perception to neural processing and metabolic execution during feeding. This study provides the first cross-tissue molecular atlas of feeding regulation in B. areolata, offering new insights into neuro-metabolic integration in gastropods and informing feed optimization and health-oriented aquaculture strategies.