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.

Pollution and other anthropogenic effects have driven a decrease in Atlantic salmon (Salmo salar) in the Iberian Peninsula. The restocking effort carried out in the 1980s, with salmon from northern latitudes with the aim of mitigating the decline of native populations, failed, probably due to the deficiency in adaptation of foreign salmon from northern Europe to the warm waters of the Iberian Peninsula. This result would imply that the Iberian populations of Atlantic salmon have experienced local adaptation in their past evolutionary history, as has been described for other populations of this species and other salmonids. Local adaptation can occur by divergent selections between environments, favoring the fixation of alleles that increase the fitness of a population in the environment it inhabits relative to other alleles favored in another population. In this work, we compared the genomes of different populations from the Iberian Peninsula (Atlantic and Cantabric basins) and Scotland in order to provide tentative evidence of candidate SNPs responsible for the adaptive differences between populations, which may explain the failures of restocking carried out during the 1980s. For this purpose, the samples were genotyped with a 220,000 high-density SNP array (Affymetrix) specific to Atlantic salmon. Our results revealed potential evidence of local adaptation for North Spanish and Scottish populations. As expected, most differences concerned the comparison of the Iberian Peninsula with Scotland, although there were also differences between Atlantic and Cantabric populations. A high proportion of the genes identified are related to development and cellular metabolism, DNA transcription and anatomical structure. A particular SNP was identified within the NADP-dependent malic enzyme-2 (mMEP-2*), previously reported by independent studies as a candidate for local adaptation in salmon from the Iberian Peninsula. Interestingly, the corresponding SNP within the mMEP-2* region was consistent with a genomic pattern of divergent selection.

The Atlantic salmon shows strong population structure with reduced gene flow, owing to homing behaviour. Supportive breeding with allochtonous parr or fish‐farm escapees could affect native population genetic structure by the introgression of foreign genes. Mature male parr are potentially powerful vehicles for promoting introgression: they can fertilize eggs in competition with anadromous males. As a consequence, foreign males contribute more to introgression than foreign females. This effect must be taken into account for the correct development of conservation programmes. Foreign males constitute an inadvertent way to disrupt the genetic structure, as the allochtonous parr or fish‐farm escapees can survive in the river during the parr stage. A short polymorphic fragment of the sex‐determining gene (sdY) was used as a marker to assess introgression via males into south European salmon populations. In order to find haplotype variants for the intronic sequence of sdY, samples were investigated from 16 different rivers across the distribution range of the salmon, together with historical samples (1950–1960) from three Spanish rivers. Two novel haplotypes, in addition to the three already described in Atlantic salmon, were found for this locus. Most samples, including historical ones, displayed the common haplotype (D) previously found in salmon all over Europe; however, north European haplotype variants were also detected in salmon inhabiting the southern European rivers that were systematically supplemented with foreign stocks between 1981 and 1994. Analysis of haplotype variation in the sdY intron constitutes a powerful and inexpensive tool, not only to specifically assess male‐mediated introgression into natural populations of Atlantic salmon, but also for monitoring salmon escapees.