Comparative Transcriptomics Provides Insight into the Neuroendocrine Regulation of Spawning in the Black-Lip Rock Oyster (Saccostrea echinata)

Abstract

The black-lip rock oyster, Saccostrea echinata, is an emerging aquaculture species; however, difficulties in regulating their gonad conditioning to full maturation and spawning have impacted industry progress. Addressing this challenge requires a deeper understanding of the molecular mechanisms underlying reproduction, particularly the signalling molecules (e.g., neuroendocrine hormones) that regulate gonad development and spawning, which remains poorly understood in this species. Therefore, we investigated the molecular neuroendocrine regulation of gonad maturation in S. echinata through the analysis of gonad histological changes correlated with gene expression in the visceral ganglia and gonad (of male and female) at pre- and post-spawn stages. Our targeted analysis of neuropeptide genes demonstrated that only LASGLVamide showed significant differential expression, being upregulated in the pre-spawn female gonad. Of the 26 reproductive-related genes identified, four were significantly upregulated in female gonad (SOX9, Dax1, Nanos-like, and Piwi-like), while an insulin-like peptide receptor was elevated in male visceral ganglia at post-spawn. Untargeted investigation revealed numerous transmembrane receptors significantly upregulated in the pre-spawn ovary, such as receptors for thyrotropin-releasing hormone, metabotropic glutamate, and 5-hydroxytryptamine, while mesotocin and oxytocin receptors were upregulated in pre-spawn male gonads. At the post-spawn stage, the visceral ganglia displayed upregulation of genes encoding stress-related proteins such as superoxidase dismutase and DnaJ homologue subfamily A member 1. These findings provide important insights into the complexities of neuroendocrine signalling molecules and establish a molecular foundation to guide selective breeding and broodstock management strategies that will support sustainable aquaculture development of black-lip rock oyster.