High water temperature impairs ovarian activity and gene expression in the brain–pituitary–gonadal axis in female red seabream during the spawning season

•High water temperature impairs gonadal activity in red seabream.•An increase in temperature leads to termination of the spawning season.•High temperature suppresses FSH, LH, GnRH1, and GnRH-R gene expression.

Temperature plays a pivotal role in the control of seasonal reproduction in temperate fish species. It is well known that temperatures that exceed a certain threshold impair gonadal development, maturation, and spawning. However, the endocrine mechanisms that underlie these effects are poorly understood. We evaluated the effect of high water temperature on the brain–pituitary–gonadal (B–P–G) axis of a perciform fish, red seabream, Pagrus (Chrysophrys) major during its spawning season (April–May). Fish were reared at either high (24 °C: H-group) or optimal/control (17 °C: C-group) temperatures for 5 or 10 d. After 5 d, the transcript abundance of gonadotropin-releasing hormone-1 (GnRH1) in the brain and GnRH receptor (GnRH-R) and FSH-β in the pituitary were significantly lower in H-group than in C-group. Conversely, there was no difference in pituitary LH-β mRNA levels, serum concentrations of estradiol-17β (E2), or the gonadosomatic index (GSIs) between H- and C-groups on Day 5. After 10 d, the ovaries of all H-group fish had completely regressed and were filled with only perinucleolar stage primary oocytes and atretic oocytes. The brain GnRH1 expression, pituitary GnRH-R and pituitary LH-β expression, serum E2 concentrations, and the GSI were significantly lower in the H-group on Day 10. Our results suggest that high water temperature is the proximate driver of the termination of the spawning season of female red seabream. The effect appears to be mediated by suppression of gene expression in the B–P–G axis.