Characterization of transcriptomic profiles underlying gross morphological changes observed in semelparous pink salmon (Oncorhynchus gorbuscha)

Pacific salmon undergo dramatic physiological remodeling during their terminal spawning migration, culminating in reproductive maturation, senescence, and death. To investigate the molecular mechanisms underlying these processes, we characterized transcriptomic changes in wild pink salmon (Oncorhynchus gorbuscha) sampled at three migratory stages (marine, riverine, and spawning ground) and across three tissues central to endocrine regulation and energy metabolism: gonads, head kidney, and skeletal muscle. Differential gene expression analysis was performed to identify biological pathways associated with maturation and semelparity. Transcriptomic changes were most pronounced during the final transition from river migrating fish to spawning, with the gonads exhibiting the greatest number of differentially expressed genes, followed by skeletal muscle and head kidney. Gene ontology analyses revealed coordinated upregulation of pathways associated with starvation responses, lipid mobilization, tissue catabolism, proteolysis, autophagy, and cell death across tissues. Immune and inflammatory processes were elevated in skeletal muscle and head kidney, while gonads showed strong enrichment of insulin signaling, steroid metabolism, and hormone-response pathways. Analysis of endocrine receptor expression identified tissue-specific and ohnolog-specific regulation of receptors involved in thyroid, growth hormone, insulin, gonadotropin, sex steroid, and glucocorticoid signaling, suggesting functional divergence among duplicated salmonid genes. These findings identified in pink salmon provide evidence for strong maturity induced molecular changes occurring at the time of final maturation rather than freshwater entry. The coordinated activation of endocrine, metabolic, and degenerative pathways supports a mechanistic link between reproductive development and semelparous senescence, providing new insight into the endocrine networks that govern spawning-associated physiological decline in Pacific salmon.