Abstract
Reproductive homing migration of salmonids requires accurate interaction between the reception of external olfactory cues for navigation to the spawning grounds and the regulation of sexual maturation processes. This study aimed at providing insights into the hypothesized functional link between olfactory sensing of the spawning ground and final sexual maturation. We have therefore assessed the presence and expression levels of olfactory genes by RNA sequencing (RNAseq) of the olfactory rosettes in homing chum salmon Oncorhynchus keta Walbaum from the coastal sea to 75 km upstream the rivers at the pre-spawning ground. The progression of sexual maturation along the brain-pituitary-gonadal axis was assessed through determination of plasma steroid levels by time-resolved fluoroimmunoassays (TR-FIA), pituitary gonadotropin subunit expression and salmon gonadotropin-releasing hormone (sgnrh) expression in the brain by quantitative real-time PCR. RNAseq revealed the expression of 75 known and 27 unknown salmonid olfactory genes of which 13 genes were differentially expressed between fish from the pre-spawning area and from the coastal area, suggesting an important role of these genes in homing. A clear progression towards final maturation was characterised by higher plasma 17α,20β-dihydroxy-4-pregnen-3-one (DHP) levels, increased pituitary luteinizing hormone β subunit (lhβ) expression and sgnrh expression in the post brain, and lower plasma testosterone (T) and 17β-estradiol (E2) levels. Olfactomedins and ependymin are candidates among the differentially expressed genes that may connect olfactory reception to the expression of sgnrh to regulate final maturation.
Highlights
Reproductive homing migration, especially long distance semelparous migration, requires accurate interaction between the external and the internal environment, that is, between homing cues and the reproductive axis
Chum salmon that were caught in the coastal sea at Ishikari Bay had a body-weight (BW) of 2,842 ± 217 g and were not significantly different in size from those caught at the pre-spawning ground in Chitose River that weighted 2,940 ± 186 g
Females caught at the pre-spawning ground were shorter than those caught in the coastal sea which caused the overall difference in length between both groups
Summary
Reproductive homing migration, especially long distance semelparous migration, requires accurate interaction between the external and the internal environment, that is, between homing cues and the reproductive axis. We aimed at lifting the veil of the molecular basis of this process and the potential messengers to the reproductive axis, and at confirming the maturation status by assessing the changes that occur in the reproductive axis by tracing back signals from the maturing gonad and steroid messengers in the blood plasma, to the gonadotropins in the pituitary and to their regulation in the brain. This will be necessary to elucidate the molecular mechanisms and to investigate cause-effect relationships between the olfactory transcriptome and the sexual maturation stage in follow-up studies
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