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

Abstract

Pacific salmon (Oncorhynchus spp.) undergo intricate physiological changes during maturation as they migrate to spawning beds and breed before succumbing to a programmed senescence (semelparous life cycle). Research into the physiological mechanisms of semelparity in salmon has identified a clear and progressive rise in sex and stress hormone levels throughout their migration, which correlates with the emergence of morphological traits, as well as changes in behavioral patterns. We examined transcriptional changes in three critical tissues (gonads, head kidney, and skeletal muscle) across the spawning migration in male and female Pink salmon (Oncorhynchus gorbuscha) to capture the molecular changes occurring in these tissues during maturation and senescence. Major transcriptional changes occurred around the time of spawning, while only modest transcriptional changes were found as the fish migrated between saltwater and freshwater. Examination of enriched biological pathways identified the signatures of semelparous catabolic processes in all tissues and a strong immune response in somatic tissues. Evidence of shifts in lipid energy mobilization were also seen in somatic tissues. A closer investigation of the expression patterns of endocrine hormone receptors showed that many endocrine pathways prioritized expression of specific dominant ohnologs to orchestrate much of the hormone response in the analyzed tissues. Our characterization of the transcriptional profiles in migrating pink salmon adds critical context to link the molecular changes occurring in tissues to the physiological transitions that define semelparous maturation in Pacific salmon. NEW & NOTEWORTHYLarge transcriptional changes occurred in the gonads, head kidney, and skeletal muscle of pink salmon during the final stages of their spawning migration. Across the tissues and sexes, spawning was marked by coordinated activation of catabolic programs (autophagy, proteolysis, cell death), and a strong immune response in somatic tissues, alongside lipid mobilization. Endocrine receptor expression analyses revealed that the response to hormones was primarily mediated by a limited number of dominant ohnologs.