Morphogenesis, Nutrient Sources, and Molecular Regulation of Metamorphosis from Glochidium to Juvenile Stages in the Freshwater Mussel Sinanodonta woodiana (Lea, 1834)

Freshwater mussels (Bivalvia, Unionidae) are now among the world’s most imperiled taxonomic groups, and their diversity is under serious threat. The metamorphosis of glochidia parasitizing on a host fish into juveniles is undoubtedly the most unique and critical stage in the life cycle of freshwater mussels, but the underlying mechanisms remain unclear. Here, we integrated microscopic observation, stable isotope (δ13C and δ15N) tracing, and transcriptomic analysis to investigate this process in the globally distributed freshwater mussel Sinanodonta woodiana on yellow catfish (Pelteobagrus fulvidraco). Compared with glochidia, juveniles exhibited byssus abandonment and the formation of a foot, visceral mass, and new shell. The shell length (0.34 ± 0.02 mm) and height (0.31 ± 0.01 mm) of the juveniles were both larger than those of the glochidia (0.26 ± 0.01 mm and 0.30 ± 0.01 mm, respectively) (p < 0.05); however, this growth likely occurred after excystment from the host fish rather than during the parasitic phase. Juveniles showed significantly higher δ13C (−17.70 ± 0.26‰) and δ15N (9.80 ± 0.90‰) than glochidia (δ13C: −23.58 ± 0.63‰; δ15N: 6.18 ± 0.37‰) (p < 0.05), with juvenile δ15N comparable to host fish tissues. Metamorphosis generated 12,584 differentially expressed genes, mainly enriched in upregulated neuroactive ligand–receptor interaction, Ras signaling, and calcium signaling pathways. This study reveals the mechanisms of S. woodiana metamorphosis, providing valuable insights for improving breeding and thus supporting the diversity conservation of freshwater mussels.