Development of supermale and all-male Atlantic salmon to research the vgll3 allele - puberty link

Abstract

Background Farmed Atlantic salmon are one of the most economically significant global aquaculture products. Early sexual maturation of farmed males represents a significant challenge to this industry and has been linked with the vgll3 genotype. However, tools to aid research of this topic, such as all-male and clonal fish, are still lacking. The present 6-year study examined if all-male production is possible in Atlantic salmon, a species with heteromorphic sex chromosomes (males being XY, females XX), and if all-male fish can be applied to further explore the vgll3 contribution on the likelihood of early maturation. Results Estrogen treatment of mixed sex yolk sac larvae gave rise to one sexually mature hermaphrodite with a male genotype (XY) that was used to produce both self-fertilized offspring and androgenetic double haploid (dh) offspring following egg activation with UV treated sperm and pressure shock to block the first mitotic division. There were YY supermales among both offspring types, which were crossed with dh females. Between 1 and 8% of the putative all-male offspring from the eight crosses with self-fertilized supermales were found to have ovaries, and 95% of these phenotypic females were also genetically female. None of the offspring from the one dh supermale cross had ovaries. When assessing the general contribution of the vgll3 locus on the likelihood of early post-smolt sexual maturation (jacking) in the all-male populations we found individuals that were homozygous for the early maturing genotype (97%) were more likely to enter puberty than individuals that were homozygous for the late maturing genotype (26%). However, the likelihood of jacking within individuals with an early/late heterozygous genotype was higher when the early allele came from the dam (94%) compared to the sire (45%). Conclusions The present results show that supermale Atlantic salmon are viable and fertile and can be used as a research tool to study important aspects of sexual maturation, such as to further explore the sex dependent parental genetic contribution to age at puberty in Atlantic salmon. In addition, we report the production of viable double haploid supermale fish.

Polygenic and major‐locus contributions to sexual maturation timing in Atlantic salmon

“…Contrary to previous assumptions that life‐history traits are polygenic traits (Lande, 1982; Roff, 2002), usually coded by many loci with small effect (Hill, 2010; Lynch & Walsh, 1998), major locus effects on life histories are being identified in an increasing number of species (e.gCheng et al, 2018; Pearse et al, 2019; Wang et al, 2018). In Atlantic salmon ( Salmo salar ), a single locus ( vgll3 ) explained a large proportion of phenotypic variation for maturation age (33%–39%; Ayllon et al, 2015; Barson et al, 2015), and for maturation probability at a specific age (Fjelldal et al, 2020). The vgll3 locus has been reported to show sex‐specific dominance for sea age at maturity in two previous studies (Barson et al, 2015; Czorlich et al,2018), with dominance of the “early” allele ( vgll3 *E) in males and dominance of the “late” allele ( vgll3 *L) in females.…”

Pituitary Gonadotropin Gene Expression During Induced Onset of Postsmolt Maturation in Male Atlantic Salmon: In Vivo and Tissue Culture Studies

“…Pituitaries from sibling salmon males with low genetic variation ( 31 ) and sharing the same genetic predisposition to mature ( 29 , 30 ), were analyzed by RNAseq to investigate global gene expression of pituitary tissue upon entering puberty. To this end, juvenile males were exposed to stimulatory photoperiod and water temperature conditions (constant light and 16°C, as described above) for 11 days and samples were collected after 7 and 11 days.…”

“…Group 4 . All-male siblings, heterozygous for the puberty-associated vgll3 locus ( 29 , 30 ), were produced by crossing a double haploid XX female with a YY supermale ( 31 ). At the age of 14-15 months, the fish were exposed to stimulatory conditions for 6 months.…”

“…We used immature sibling salmon males for the RNAseq study, which showed a low genetic variation since they were produced by crossing a double haploid XX female with an inbreed YY supermale, created by self-fertilization from a hermaphrodite ( 31 ). These immature fish, heterozygous for the puberty-associated vgll3 locus, were exposed to constant light and 16°C.…”

Effects of Early Thermal Environment on Growth, Age at Maturity, and Sexual Size Dimorphism in Arctic Charr

“…Males and females within each temperature group were sorted into three maturation stages based on their GSI at harvest. In accordance with the GSI of immature male Atlantic salmon [31], males having GSI < 0.2% were categorized as immature. Male maturation stages were based on the GSI frequency distributions within the 10C and 12C groups.…”