Differential pituitary mRNA expression in wild and hatchery-produced greater amberjack Seriola dumerili exhibiting normal and impaired spermatogenesis

The greater amberjack Seriola dumerili is a promising aquaculture species in the Mediterranean Sea. However, first generation (F1) hatchery-produced individuals exhibit reproductive dysfunctions when reared in tanks or in cages. As part of a broader investigation into the impacts of captivity, we compared the pituitary transcriptomes of wild and F1 greater amberjack during spermatogenesis. Wild males (WILD group, n = 4) displayed normal testicular development; among F1 males, some had normal testicular development (NormalF, n = 4), while others showed spermatogenesis impairment (DysF, n = 2). Transcriptomic analysis revealed 301 differentially expressed genes (DEGs) in the DysF vs. WILD comparison and 376 DEGs in the NormalF vs. WILD comparison, while no DEGs were detected between DysF and NormalF. Protein-protein interaction (PPI) analysis identified regulatory networks involving 246 proteins across eleven functional categories in DysF vs. WILD, and 382 proteins across 10 categories in NormalF vs. WILD. Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis showed DEGs enriched in 62 (DysF vs. WILD) and 84 (NormalF vs. WILD) pathways. Notably, several dysregulated pathways common to all F1 males are associated with reproductive functions, as well as nucleotide metabolism, calcium signaling, MAPK and mTOR signaling, neuroactive ligand-receptor interaction, Gonadotropin Releasing Hormone (GnRH) and ErbB signaling pathways. Among the DEGs, some genes were linked to GnRH neuron migration, panhypopituitarism and hypogonadotropic hypogonadism. These findings suggest that reproductive dysfunctions in F1 male greater amberjack may involve a suppression of pituitary activity mediated by dysregulation of the opioid, endocannabinoid and dopaminergic systems.