Environmental and Genetic (vgll3) Effects on the Prevalence of Male Maturation Phenotypes in Domesticated Atlantic Salmon

Abstract

Pre-harvest male maturation is problematic for Atlantic salmon (Salmo salar) farmers and is regulated by the environment and genetics (e.g., vgll3). Five families of all-male salmon parr (produced using YY males crossed with XX females) with different vgll3 genotypes were split between three environmental regimes in January 2018. The “advanced maturation” regime used elevated temperature (16 °C) and continuous light from January 2018 with post-smolt maturation assessed in March 2018. The “extended freshwater” regime used ambient freshwater (1–16 °C) and simulated natural photoperiod (SNP) with post-smolt maturation assessed in November 2018. The “sea transfer” regime used ambient temperatures (1–14 °C) and SNP in freshwater until May 2018 when they were transferred to 9 °C seawater with natural photoperiod for 2.5 years (final mean weight of circa. 14 kg) and assessed for post-smolt maturation, 1 sea-winter (1 SW) maturation, and 2 sea-winter (2 SW) maturation in the autumn (November/December) of 2018, 2019, and 2020, respectively. Post-smolt maturation was highest in the advanced maturation and extended freshwater regimes (39–99% depending on family) and lowest in the sea transfer regime (0–95% depending on family). In the sea transfer regime, maturity incidence increased over time (0–95% post-smolt maturation, 1–100% 1 SW, and 50–90% 2 SW maturation, depending on family). In all regimes, those homozygous for the pre-designated vgll3 “early” maturing allele had the highest incidences of maturation whilst those homozygous for the “late” allele had the lowest. A low percentage of 2 SW phenotypic and genetic females were found (0–5% depending on family), one of which was successfully crossed with an XY male resulting in progeny with an approx. 50/50 sex ratio. These results show (i) post-smolt maturation varies dramatically depending on environment although genetic regulation by vgll3 was as expected, and (ii) crossing YY sperm with XX eggs can result in XX progeny which can themselves produce viable progeny with an equal sex ratio when crossed with an XY male.