Wild and domesticated Atlantic salmon males display large variation for sea age at sexual maturation, which varies between 1–5 years. Previous studies have uncovered a genetic predisposition for variation of age at maturity with moderate heritability, thus suggesting a polygenic or complex nature of this trait. The aim of this study was to identify associated genetic loci, genes and ultimately specific sequence variants conferring sea age at maturity in salmon. We performed a genome wide association study (GWAS) using a pool sequencing approach (20 individuals per river and phenotype) of male salmon returning to rivers as sexually mature either after one sea winter (2009) or three sea winters (2011) in six rivers in Norway. The study revealed one major selective sweep, which covered 76 significant SNPs in which 74 were found in a 370 kb region of chromosome 25. Genotyping other smolt year classes of wild and domesticated salmon confirmed this finding. Genotyping domesticated fish narrowed the haplotype region to four SNPs covering 2386 bp, containing the vgll3 gene, including two missense mutations explaining 33–36% phenotypic variation. A single locus was found to have a highly significant role in governing sea age at maturation in this species. The SNPs identified may be both used as markers to guide breeding for late maturity in salmon aquaculture and in monitoring programs of wild salmon. Interestingly, a SNP in proximity of the VGLL3 gene in humans (Homo sapiens), has previously been linked to age at puberty suggesting a conserved mechanism for timing of puberty in vertebrates.

Each year, hundreds of thousands of domesticated farmed Atlantic salmon escape into the wild. In Norway, which is the world’s largest commercial producer, many native Atlantic salmon populations have experienced large numbers of escapees on the spawning grounds for the past 15–30 years. In order to study the potential genetic impact, we conducted a spatio-temporal analysis of 3049 fish from 21 populations throughout Norway, sampled in the period 1970–2010. Based upon the analysis of 22 microsatellites, individual admixture, FST and increased allelic richness revealed temporal genetic changes in six of the populations. These changes were highly significant in four of them. For example, 76% and 100% of the fish comprising the contemporary samples for the rivers Vosso and Opo were excluded from their respective historical samples at P = 0.001. Based upon several genetic parameters, including simulations, genetic drift was excluded as the primary cause of the observed genetic changes. In the remaining 15 populations, some of which had also been exposed to high numbers of escapees, clear genetic changes were not detected. Significant population genetic structuring was observed among the 21 populations in the historical (global FST = 0.038) and contemporary data sets (global FST = 0.030), although significantly reduced with time (P = 0.008). This reduction was especially distinct when looking at the six populations displaying temporal changes (global FST dropped from 0.058 to 0.039, P = 0.006). We draw two main conclusions: 1. The majority of the historical population genetic structure throughout Norway still appears to be retained, suggesting a low to modest overall success of farmed escapees in the wild; 2. Genetic introgression of farmed escapees in native salmon populations has been strongly population-dependent, and it appears to be linked with the density of the native population.

BackgroundMany native Atlantic salmon populations have been invaded by domesticated escapees for three decades or longer. However, thus far, the cumulative level of gene-flow that has occurred from farmed to wild salmon has not been reported for any native Atlantic salmon population. The aim of the present study was to investigate temporal genetic stability in native populations, and, quantify gene-flow from farmed salmon that caused genetic changes where they were observed. This was achieved by genotyping historical and contemporary samples from 20 populations covering all of Norway with recently identified single nucleotide polymorphism markers that are collectively diagnostic for farmed and wild salmon. These analyses were combined with analysis of farmed salmon and implementation of Approximate Bayesian computation based simulations.ResultsFive of the populations displayed statistically significant temporal genetic changes. All five of these populations became more similar to a pool of farmed fish with time, strongly suggesting introgression of farmed fish as the primary cause. The remaining 15 populations displayed weak or non-significant temporal genetic changes. Estimated introgression of farmed fish ranged from 2-47% per population using approximate Bayesian computation. Thus, some populations exhibited high degrees of farmed salmon introgression while others were more or less unaffected. The observed frequency of escapees in each population was moderately correlated with estimated introgression per population R2 = 0.47 P < 0.001. Genetic isolation by distance existed within the historical and contemporary data sets, however, the among-population level of divergence decreased with time.ConclusionsThis is the first study to quantify cumulative introgression of farmed salmon in any native Atlantic salmon population. The estimations demonstrate that the level of introgression has been population-specific, and that the level of introgression is not solely predicted by the frequency of escapees observed in the population. However, some populations have been strongly admixed with farmed salmon, and these data provide policy makers with unique information to address this situation.

Atlantic salmon (Salmo salar) is an economically and culturally important species. Norway has more than 400 watercourses with Atlantic salmon and supports a large proportion of the world's wild Atlantic salmon. Atlantic salmon are structured into numerous genetically differentiated populations, and are therefore managed at the population level. Long-distance migrations between freshwater and ocean habitats expose Atlantic salmon to multiple threats, and a number of anthropogenic factors have contributed to the decline of Atlantic salmon during the last decades. Knowledge on the relative importance of the different anthropogenic factors is vital for prioritizing management measures. We developed a semi-quantitative 2D classification system to rank the different anthropogenic factors and used this to assess the major threats to Norwegian Atlantic salmon. Escaped farmed salmon and salmon lice from fish farms were identified as expanding population threats, with escaped farmed salmon being the largest current threat. These two factors affect populations to the extent that they may be critically endangered or lost, with a large likelihood of causing further reductions and losses in the future. The introduced parasite Gyrodactylus salaris, freshwater acidification, hydropower regulation and other habitat alterations were identified as stabilized population threats, which have contributed to populations becoming critically endangered or lost, but with a low likelihood of causing further loss. Other impacts were identified as less influential, either as stabilized or expanding factors that cause loss in terms of number of returning adults, but not to the extent that populations become threatened. Management based on population specific reference points (conservation limits) has reduced exploitation in Norway, and overexploitation was therefore no longer regarded an important impact factor. The classification system may be used as a template for ranking of anthropogenic impact factors in other countries and as a support for national and international conservation efforts.

A large number of farmed Atlantic salmon escape from sea cages and hatcheries annually. Selection programmes and domestication have changed the genetic composition of farmed salmon to improve their performance in the culture environment, which apparently occurs at the cost of their fitness in the natural environment. Therefore, gene flow from farmed salmon to wild salmon populations may have altered the genetic composition of wild salmon populations. To investigate the temporal genetic stability in seven wild Norwegian salmon populations, genetic profiles were produced from historical and contemporary scale samples. Historical and contemporary samples of salmon from the Namsen, Etne, Opo, Vosso, Granvin, Eio, and Hå Rivers were genotyped at the following eight microsatellite loci: Ssa13.37, Ssa28, SsOSL85, Ssa197, Ssa20.19, SsaF43, Ssa202, and Ssa85. A significant change in genetic profiles was observed over time in the Opo, Vosso, and Eio Rivers, but no changes in genetic profiles were observed in the Namsen, Etne, Granvin, and Hå Rivers. A small reduction in FST values and genetic distances among populations was observed in the contemporary samples compared with the historical samples, indicating a eduction in population differentiation over time.