Evolution of Sex Determination Loci in Atlantic Salmon

Abstract

Teleost fish exhibit a remarkable diversity in the control of sex determination, offering the opportunity to identify novel differentiation mechanisms and their ecological consequences. Here, we perform GWAS using 4715 fish and 46,501 SNP to map sex determination to three separate genomic locations in Atlantic salmon (Salmo salar). To characterize each, whole genome sequencing was performed to 30-fold depth of coverage using 20 fish representing each of three identified sex lineages. SNP polymorphism reveals male fish carry a single copy of the male specific region, consistent with an XX/XY or male heterogametric sex system. Haplotype analysis revealed deep divergence between the putatively ancestral locus on chromosome 2, compared with loci on chromosomes 3 and 6. Haplotypes in fish carrying either the chromosome 3 or 6 loci were nearly indistinguishable, indicating a founding event that occurred following the speciation event that defined Salmo salar from other salmonids. These findings highlight the evolutionarily fluid state of sex determination systems in salmonids, and resolve to the sequence level differences in animals with divergent sex lineages.

Sex determining gene transposition as an evolutionary platform for chromosome turnover

“…These originated from 3 dams and 5 sires among the 88 parents. The number of discordant females observed here is higher than the 1% frequency observed in a domesticated Tasmanian Atlantic salmon strain (Eisbrenner et al 2014;Kijas et al 2018). Given the inheritance model presented here, it is likely that this difference is merely the result of the number of affected parents and the cross design, although strain specific differences in the frequency of the pseudocopy of sdY cannot be ruled out.…”

“…The above observations are consistent with the findings of the present study where sdY was mapped to 2, 3 and 6 in the 64 families. In all these studies, chromosome 2 is identified as the most common location for sdY and is likely to be the ancestral variant (Kijas et al 2018). Surprisingly, low divergence between the Ssa03 and Ssa06 loci has been reported (Kijas et al 2018), suggesting a recent origin even though these variants are present in both the North American and European lineages.…”

“…In all these studies, chromosome 2 is identified as the most common location for sdY and is likely to be the ancestral variant (Kijas et al 2018). Surprisingly, low divergence between the Ssa03 and Ssa06 loci has been reported (Kijas et al 2018), suggesting a recent origin even though these variants are present in both the North American and European lineages. Convergent sex chromosome turnover might be the product of sdY transposable nature (Faber-Hammond, Phillips, and Brown 2015) and gene landscape (Bertho et al 2018).…”

“…Within Atlantic salmon, sdY has been mapped to chromosomes Ssa02, Ssa03 and Ssa06 in a domesticated strain of salmon originating from North America, and, in both wild and domesticated Norwegian strains (Eisbrenner et al 2014;Kijas et al 2018;Besnier et al 2020).…”

“…Nevertheless, the mechanisms underpinning this discordance are unknown. Adding to the complexity of the situation is the fact that sdY has been mapped to different regions of the genome in the various salmonid species, but also within the same species, suggesting that it transposes to a new location either at the time of speciation (Phillips 2013) or more recently (Kijas et al 2018). Specifically within Atlantic salmon, sdY has been mapped to chromosomes Ssa02, Ssa03, Ssa06 and possibly Ssa21 (Eisbrenner et al 2014;Lubieniecki et al 2015;Kijas et al 2018;Gabian et al 2019).…”