Estrogen therapy offsets thermal impairment of vitellogenesis, but not zonagenesis, in maiden spawning female Atlantic salmon (Salmo salar)

Abstract

In female Atlantic salmon (Salmo salar), exposure to warm summer temperatures causes a reduction in plasma 17β-estradiol (E2), which impairs downstream vitellogenesis and zonagenesis, and reduces egg fertility and embryo survival. The aim of the present study was to determine whether E2-treatment could offset thermal impairment of endocrine function and maintain egg quality in maiden (first-time-spawning) S. salar reared at 22 °C. Treatment with E2 at 22 °C stimulated vitellogenin (vtg) gene expression and subsequent protein synthesis which promoted oocyte growth and increased egg size relative to untreated fish at 14 and 22 °C. However, E2-treatment at 22 °C was not associated with an increase in egg fertility and embryo survival relative to untreated fish at 22 °C, despite the positive effects of E2-treatment on vitellogenesis and oocyte growth. As there was no evidence to suggest that the estrogen receptor alpha expression was suppressed by high temperature, this could be due to the lack of stimulation on zonagenesis by E2-treatment observed at high temperature during oocyte development. Our results demonstrate that treatment with E2 is not able to maintain zonagenesis or egg quality in maiden S. salar at high temperature, even when vtg gene expression, protein synthesis and subsequent oocyte growth is promoted. This implies that the mechanisms regulating zonagenesis, but not vitellogenesis are impaired at elevated temperature in female S. salar broodstock, and highlights the remarkable complexity of thermally induced endocrine disruption in fish.

Keywords: Aquaculture; Climate change; Gene expression; Hormonal therapy; Ovarian steroidogenesis; Salmon; Temperature.

Figure 1. Thermal treatment regimes, hormone pellet implant dates (indicated by asterisk) and sampling times (1–4) for maiden S. salar held at 14 or 22 °C in late summer and autumn.

Figure 2. Gonadosomatic index (A) and follicle diameters (B) among maiden S. salar without hormone pellet implants held at 14 or 22 °C, and with E2 pellet implants held at 22 °C.

Values are means + SE (n = 7 unless stated otherwise). Different alphabetical superscripts at each sample time denote significant differences (P < 0.05). Other details as for Fig. 1.

Figure 3. Absolute (A) and relative fecundity (B) and the proportions of atretic follicles (C) in the ovaries of maiden S. salar without hormone pellet implants held at 14 (open bars), or 22 °C (cross-hatched bars), and fish with E2 pellet implants held at 22 °C (black bars).

Values are means + SE (n = 7 unless stated otherwise). Different alphabetical superscripts at each sample time denote significant differences (P < 0.05) except for % atresia at sample time 4 (*P < 0.057; F = 3.486). Other details as for Fig. 1.

Figure 4. Cumulative ovulation in maiden S. salar spawners without hormone pellet implants held at 14 and 22 °C, and fish with E2 pellet implants held at 22 °C during autumn.

Figure 5. Post-ovulatory fecundity (A, B), oocyte diameter (C) and volume (D), fertility (E), and survival to eyed egg stage (F) among maiden S. salar without hormone pellet implants held at 14 or 22 °C, and with E2 pellet implants held at 22 °C.

Values are mean + SE (or 95% confidence limits for % data) (n = 7, 5 and 3 for the three groups respectively; n = 1 for eyed egg survival in 22 °C + pellet group). Different alphabetical superscripts among sample times denote significant differences (P < 0.05) unless stated otherwise.

Figure 6. Plasma levels of estradiol (A), testosterone (B), cortisol (C) and vitellogenin (D) among maiden S. salar spawners without hormone pellet implants held at 14 (open bars) or 22 °C (cross-hatched bars), and fish with E2 pellet implants held at 22 °C (black bars).

Values are means + SE (n = 7 unless stated otherwise). Different alphabetical superscripts among sample times denote significant differences (P < 0.05). Other details as for Fig. 1.

Figure 7. Relative gene expression of vitellogenin (A), estrogen receptor α (B), zona pellucida c and b (C and D) among maiden S. salar without hormone pellet implants held at 14 or 22 °C, and with E2 pellet implants held at 22 °C.

Values are means + SE (n = 7 unless stated otherwise). Different alphabetical superscripts among sample times denote significant differences (P < 0.05). Other details as for Fig. 1.