Identification of genomic regions regulating sex determination in Atlantic salmon using high density SNP data

Abstract

BackgroundA complete understanding of the genetic basis for sexual determination and differentiation is necessary in order to implement efficient breeding schemes at early stages of development. Atlantic salmon belongs to the family Salmonidae of fishes and represents a species of great commercial value. Although the species is assumed to be male heterogametic with XY sex determination, the precise genetic basis of sexual development remains unclear. The complexity is likely associated to the relatively recent salmonid specific whole genome duplication that may be responsible for certain genome instability. This instability together with the capacity of the sex-determining gene to move across the genome as reported by previous studies, may explain that sexual development genes are not circumscribed to the same chromosomes in all members of the species. In this study, we have used a 220 K SNP panel developed for Atlantic salmon to identify the chromosomes explaining the highest proportion of the genetic variance for sex as well as candidate regions and genes associated to sexual development in this species.ResultsResults from regional heritability analysis showed that the chromosomes explaining the highest proportion of variance in these populations were Ssa02 (heritability = 0.42, SE = 0.12) and Ssa21 (heritability = 0.26, SE = 0.11). After pruning by linkage disequilibrium, genome-wide association analyses revealed 114 SNPs that were significantly associated with sex, being Ssa02 the chromosome containing a greatest number of regions. Close examination of the candidate regions evidenced important genes related to sex in other species of Class Actinopterygii, including SDY, genes from family SOX, RSPO1, ESR1, U2AF2A, LMO7, GNRH-R, DND and FIGLA.ConclusionsThe combined results from regional heritability analysis and genome-wide association have provided new advances in the knowledge of the genetic regulation of sex determination in Atlantic salmon, supporting that Ssa02 is the candidate chromosome for sex in this species and suggesting an alternative population lineage in Spanish wild populations according to the results from Ssa21.

Sex determining gene transposition as an evolutionary platform for chromosome turnover

“…It has also been mapped to chromosomes Ssa02 and Ssa21 in six wild Spanish populations (Gabian et al 2019). 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 Atlantic salmon, the presence of the Y specific sdY gene has been invoked to be the sole genetic requirement for maleness (Yano et al 2013). Interestingly, the existence of multiple sex determining loci (Eisbrenner et al 2014;Gabian et al 2019), and sdY transposition ability (Lubieniecki et al 2015) may give support to the existence of frequent sex chromosome turnover in this species. sdY male specificity is common in salmonids, but not in all species.…”

“…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).…”

Autosomal sdY Pseudogenes Explain Discordances Between Phenotypic Sex and DNA Marker for Sex Identification in Atlantic Salmon

“…Within Atlantic salmon, sdY has been mapped to chromosomes Ssa02, Ssa03 and Ssa06 in domesticated and wild strain of salmon from North America and Norway ( Eisbrenner et al, 2014 ; Kijas et al, 2018 ; Besnier et al, 2020 ). It has also been mapped to chromosomes Ssa02 and Ssa21 in six wild Spanish populations ( Gabian et al, 2019 ). The above observations are consistent with the findings of the present study where the SD sdY was mapped to Ssa02, Ssa03, and Ssa06 in the 64 families.…”

“…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 within species ( 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 ) evidencing its transposition ability ( Lubieniecki et al, 2015 ).…”