Atlantic salmon (Salmo salar) is one of the best researched fishes, and its aquaculture plays a global role in the blue revolution. However, since the 1970s, tens of millions of farmed salmon have escaped into the wild. We review current knowledge of genetic interactions and identify the unanswered questions. Native salmon populations are typically genetically distinct from each other and potentially locally adapted. Outside Norway, introgression remains unquantified, and in all regions, biological changes and the mechanisms driving population-specific impacts remain poorly documented. Nevertheless, existing knowledge shows that the long-term consequences of introgression is expected to lead to changes in life-history traits, reduced population productivity and decreased resilience to future challenges. Only a major reduction in the number of escapees and/or sterility of farmed salmon can eliminate further impacts. K E Y W O R D Saquaculture, evolution, fish farming, fitness, genetic, hybrid

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.

One of the most important traits linked with the successful domestication of animals is reducing their sensitivity to environmental stressors in the human controlled environment. In order to examine whether domestication selection in Atlantic salmon Salmo salar L., over approximately ten generations, has inadvertently selected for reduced responsiveness to stress, we compared the growth reaction norms of 29 wild, hybrid and domesticated families reared together under standard hatchery conditions (control) and in the presence of a stressor (reduced water level twice daily). The experiment was conducted for a 14 week period. Farmed salmon outgrew wild salmon 1∶2.93 in the control tanks, and no overlap in mean weight was displayed between families representing the three groups. Thus, the elevation of the reaction norms differed among the groups. Overall, growth was approximately 25% lower in the stressed tanksl; however, farmed salmon outgrew wild salmon 1∶3.42 under these conditions. That farmed salmon maintained a relatively higher growth rate than the wild salmon in the stressed tanks demonstrates a lower responsiveness to stress in the farmed salmon. Thus, flatter reaction norm slopes were displayed in the farmed salmon, demonstrating reduced plasticity for this trait under these specific experimental conditions. For all growth measurements, hybrid salmon displayed intermediate values. Wild salmon displayed higher heritability estimates for body weight than the hybrid and farmed salmon in both environments. This suggests reduced genetic variation for body weight in the farmed contra wild salmon studied here. While these results may be linked to the specific families and stocks investigated, and verification in other stocks and traits is needed, these data are consistent with the theoretical predictions of domestication.

Migrations between different habitats are key events in the lives of many organisms. Such movements involve annually recurring travel over long distances usually triggered by seasonal changes in the environment. Often, the migration is associated with travel to or from reproduction areas to regions of growth. Young anadromous Atlantic salmon (Salmo salar) emigrate from freshwater nursery areas during spring and early summer to feed and grow in the North Atlantic Ocean. The transition from the freshwater ('parr') stage to the migratory stage where they descend streams and enter salt water ('smolt') is characterized by morphological, physiological and behavioural changes where the timing of this parr-smolt transition is cued by photoperiod and water temperature. Environmental conditions in the freshwater habitat control the downstream migration and contribute to within- and among-river variation in migratory timing. Moreover, the timing of the freshwater emigration has likely evolved to meet environmental conditions in the ocean as these affect growth and survival of the post-smolts. Using generalized additive mixed-effects modelling, we analysed spatio-temporal variations in the dates of downstream smolt migration in 67 rivers throughout the North Atlantic during the last five decades and found that migrations were earlier in populations in the east than the west. After accounting for this spatial effect, the initiation of the downstream migration among rivers was positively associated with freshwater temperatures, up to about 10 °C and levelling off at higher values, and with sea-surface temperatures. Earlier migration occurred when river discharge levels were low but increasing. On average, the initiation of the smolt seaward migration has occurred 2.5 days earlier per decade throughout the basin of the North Atlantic. This shift in phenology matches changes in air, river, and ocean temperatures, suggesting that Atlantic salmon emigration is responding to the current global climate changes.