Pre-fertilization gamete thermal environment influences reproductive success, unmasking opposing sex-specific responses in Atlantic salmon ( Salmo salar )

Abstract

The environment gametes perform in just before fertilization is increasingly recognized to affect offspring fitness, yet the contributions of male and female gametes and their adaptive significance remain largely unexplored. Here, we investigated gametic thermal plasticity and its effects on hatching success and embryo performance in Atlantic salmon ( Salmo salar ). Eggs and sperm were incubated overnight at 2°C or 8°C, temperatures within the optimal thermal range of this species. Crosses between warm- and cold-incubated gametes were compared using a full-factorial design, with half of each clutch reared in cold temperatures and the other in warm temperatures. This allowed disentangling single-sex interaction effects when pre-fertilization temperature of gametes mismatched embryonic conditions. Pre-fertilization temperature influenced hatch timing and synchrony, and matching sperm and embryo temperatures resulted in earlier hatching. Warm incubation benefited eggs but harmed sperm, reducing the hatching success and, overall, gametic thermal plasticity did not enhance offspring fitness, indicating vulnerability to thermal changes. We highlight the sensitivity of male gametes to higher temperatures, and that gamete acclimation may not effectively buffer against deleterious effects of thermal fluctuations. From an applied angle, we propose the differential storage of male and female gametes as a tool to enhance sustainability within the hatcheries.

Does post-ejaculatory sperm experience prior to fertilization alter offspring performance beyond paternity in an external fertilizing fish?

“…However, when embryos were incubated at high temperatures, those sired by sperm treated at high temperatures exhibited inferior performance. In contrast, Ritchie and Marshall (2015) and Graziano et al (2023) suggested that the adaptive effects of tubeworm ( Galeolaria gemineoa ) and salmon ( Salmo salar ) sperm exposure when the offspring condition aligns with the condition of sperm exposure, hinting at the epigenetic mechanisms at play. On the contrary, Kekäläinen et al (2018) present evidence of maladaptive effects on European whitefish ( Coregonus lavaretus ) offspring resulting from sperm experiences, further complicating the overall picture.…”

“…These alterations in sperm may confer advantages to offspring when they encounter similar conditions to those experienced by the sperm (Figures 1 A & B). This introduces the anticipatory hypothesis, suggesting that offspring are primed for anticipated conditions, enhancing their performance in such conditions (Burgess & Marshall, 2014; Graziano et al, 2023; Hosken et al, 2003; Marshall, 2015; Ritchie & Marshall, 2013). However, if conditions differ from those experienced by the sperm, offspring performance may not improve, as the modifications may not prove advantageous in the new context (Lymbery et al, 2021).…”