Introgression from farmed escapees affects the full life cycle of wild Atlantic salmon.
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ABSTRACT:
SUBMITTER: Bolstad GH
PROVIDER: S-EPMC8694624 | biostudies-literature | 2021 Dec
REPOSITORIES: biostudies-literature
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Introgression from farmed escapees affects the full life cycle of wild Atlantic salmon.
Bolstad Geir H GH Karlsson Sten S Hagen Ingerid J IJ Fiske Peder P Urdal Kurt K Sægrov Harald H Florø-Larsen Bjørn B Sollien Vegard P VP Østborg Gunnel G Diserud Ola H OH Jensen Arne J AJ Hindar Kjetil K
Science advances 20211222 52
After a half a century of salmon farming, we have yet to understand how the influx of genes from farmed escapees affects the full life history of Atlantic salmon (<i>Salmo salar</i> L.) in the wild. Using scale samples of over 6900 wild adult salmon from 105 rivers, we document that increased farmed genetic ancestry is associated with increased growth throughout life and a younger age at both seaward migration and sexual maturity. There was large among-population variation in the effects of intr ...[more]
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Project description: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.
| S-EPMC3765417 | biostudies-literature
Project description:In some wild Atlantic salmon populations, rapid declines in numbers of wild returning adults has been associated with an increase in the prevalence of farmed salmon. Studies of phenotypic variation have shown that interbreeding between farmed and wild salmon may lead to loss of local adaptation. Yet, few studies have attempted to assess the impact of interbreeding at the genome level, especially among North American populations. Here, we document temporal changes in the genetic makeup of the severely threatened Magaguadavic River salmon population (Bay of Fundy, Canada), a population that might have been impacted by interbreeding with farmed salmon for nearly 20 years. Wild and farmed individuals caught entering the river from 1980 to 2005 were genotyped at 112 single-nucleotide polymorphisms (SNPs), and/or eight microsatellite loci, to scan for potential shifts in adaptive genetic variation. No significant temporal change in microsatellite-based estimates of allele richness or gene diversity was detected in the wild population, despite its precipitous decline in numbers over the last two decades. This might reflect the effect of introgression from farmed salmon, which was corroborated by temporal change in linkage-disequilibrium. Moreover, SNP genome scans identified a temporal decrease in candidate loci potentially under directional selection. Of particular interest was a SNP previously shown to be strongly associated with an important quantitative trait locus for parr mark number, which retained its genetic distinctiveness between farmed and wild fish longer than other outliers. Overall, these results indicate that farmed escapees have introgressed with wild Magaguadavic salmon resulting in significant alteration of the genetic integrity of the native population, including possible loss of adaptation to wild conditions.
| S-EPMC3131974 | biostudies-literature
Project description:Gene flow between wild and domestic populations has been repeatedly demonstrated across a diverse range of taxa. Ultimately, the genetic impacts of gene flow from domestic into wild populations depend both on the degree of domestication and the original source of the domesticated population. Atlantic salmon, Salmo salar, used in North American aquaculture are ostensibly of North American origin. However, evidence of European introgression into North American aquaculture salmon has accumulated in recent decades, even though the use of diploid European salmon has never been approved in Canada. The full extent of such introgression as well as the potential impacts on wild salmon in the Northwest Atlantic remains uncertain. Here, we extend previous work comparing North American and European wild salmon (n = 5799) using a 220 K SNP array to quantify levels of recent European introgression into samples of domestic salmon, aquaculture escapees, and wild salmon collected throughout Atlantic Canada. Analysis of North American farmed salmon (n = 403) and escapees (n = 289) displayed significantly elevated levels of European ancestry by comparison with wild individuals (p < 0.001). Of North American farmed salmon sampled between 2011 and 2018, ~17% had more than 10% European ancestry and several individuals exceeded 40% European ancestry. Samples of escaped farmed salmon similarly displayed elevated levels of European ancestry, with two individuals classified as 100% European. Analysis of juvenile salmon collected in rivers proximate to aquaculture locations also revealed evidence of elevated European ancestry and larger admixture tract in comparison to individuals collected at distance from aquaculture. Overall, our results demonstrate that even though diploid European salmon have never been approved for use in Canada, individuals of full and partial European ancestry have been in use over the last decade, and that some of these individuals have escaped and hybridized in the wild.
| S-EPMC9488674 | biostudies-literature
Project description: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, F(ST) 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 F(ST) =0.038) and contemporary data sets (global F(ST) =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 F(ST) 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.
| S-EPMC3419752 | biostudies-literature
Project description:The viability of wild Atlantic salmon populations is threatened by genetic introgression from escaped farmed salmon. Farmed Atlantic salmon are genetically improved for important commercial traits and a life in captivity but are poorly adapted to the natural environment. The rate of gene flow from escaped farmed to wild salmon depends on their spawning success and on offspring survival at various life stages. We here investigate relative survival of introgressed juvenile Atlantic salmon (parr) in a river in northern Norway. The studied population has experienced genetic introgression from farmed salmon for about four generations (20 years). We followed two cohorts of parr from the year of hatching (0+) to the age of 2 years (2+). Farmed genetic introgression was quantified at the individual level and on a continuous scale using diagnostic SNPs. Population-level genetic introgression decreased from 0+ to 2+ by 64% (2011 cohort) and 37% (2013 cohort). This change was driven by a 70% (2011 cohort) and 49% (2013 cohort) lower survival from age 0+ to 2+ in introgressed parr compared to parr of wild origin. Our observations show that there is natural selection against genetic introgression with a potential cost of lower productivity.
| S-EPMC8127704 | biostudies-literature
Project description:Increased knowledge of heritable traits in Atlantic Salmon (Salmo salar) is important to overcome bottlenecks in salmonid aquaculture. Atlantic salmonid populations, both landlocked and anadromous, represent an interesting model to gain insight into anadromy related traits, most notably, the probability to smoltify. While a previous study has identified several genomic regions diverging between anadromous and landlocked populations across the species range, the present study explores these data further with the aim to uncover if some of these genomic regions are linked to beneficial genetic traits associated with smoltification. In this study 17 of these loci were monitored in 669 anadromous salmon originating from 36 full-sibling families that had been reared under common garden conditions. The Smolt Index was calculated, using multiple visual markers, and provided a means of assessing smoltification stage. One SNP, located in Ssa04, showed a significant association with probability to smoltify, where individuals homozygous for the landlocked variant (LL) displayed a decrease in probability of smoltifying after one winter when compared with the homozygous for the anadromous variant (AA). This effect was independent of individual fish size. A separate common garden study comprising 200 individuals from either anadromous or landlocked strains showed that expression levels of ncor1, a thyroid mediator hormone located on the same chromosomal region (Ssa04), were significantly reduced in landlocked individuals post smoltification but remained constant in their anadromous counterparts. This study therefore suggests that while size is still the most important trigger for the induction of smoltification, there may also be an additional genetic component or trigger that has been 'lost' during the years deprived of SW transfer. In conclusion, the LL genotype identified here could potentially be used by the industry to delay smoltification and may also represent one of the first clues to the genetic regulation of smoltification in Atlantic salmon.
| S-EPMC11363631 | biostudies-literature
Project description:Many wild Atlantic salmon (Salmo salar) populations are threatened by introgressive hybridization from domesticated fish that have escaped from aquaculture facilities. A detailed understanding of the hybridization dynamics between wild salmon and aquaculture escapees requires discrimination of different hybrid classes; however, markers currently available to discriminate the two types of parental genome have limited power to do this. Using a high-density Atlantic salmon single nucleotide polymorphism (SNP) array, in combination with pooled-sample allelotyping and an Fst outlier approach, we identified 200 SNPs that differentiated an important Atlantic salmon stock from the escapees potentially hybridizing with it. By simulating multiple generations of wild-escapee hybridization, involving wild populations in two major phylogeographic lineages and a genetically diverse set of escapees, we showed that both the complete set of SNPs and smaller subsets could reliably assign individuals to different hybrid classes up to the third hybrid (F3) generation. This set of markers will be a useful tool for investigating the genetic interactions between native wild fish and aquaculture escapees in many Atlantic salmon populations.
| S-EPMC4999531 | biostudies-literature
Project description:Domesticated Atlantic salmon grow much faster than wild salmon when reared together in fish tanks under farming conditions (size ratios typically 1:2-3). In contrast, domesticated salmon only display marginally higher growth than wild salmon when reared together in rivers (size ratios typically 1:1-1.2). This begs the question why? Is this a difference in the plastic response driven by divergent energy budgets between the two environments, or is it a result of selection, whereby domesticated salmon that display the greatest growth-potential are those at greatest risk of mortality in the wild? We reared domesticated, hybrid and wild salmon in a river until they smoltified at age 2 or 4, and thereafter in fish tanks for a further 2 years. In the river, there was no difference in the mean size between the groups. In contrast, after being transferred from the river to fish tanks, the domesticated salmon significantly outgrew the wild salmon (maximum size ratio of ~1:1.8). This demonstrates that selection alone cannot be responsible for the lack of growth differences observed between domesticated and wild salmon in rivers. Nevertheless, the final size ratios observed after rearing in tanks were lower than expected in that environment, thus suggesting that plasticity, as for selection, cannot be the sole mechanism. We therefore conclude that a combination of energy-budget plasticity, and selection via growth-potential mortality, cause the differences in growth reaction norms between domesticated and wild salmon across these contrasting environments. Our results imply that if phenotypic changes are not observed in wild populations following introgression of domesticated conspecifics, it does not mean that functional genetic changes have not occurred in the admixed population. Clearly, under the right environmental conditions, the underlying genetic changes will manifest themselves in the phenotype.
| S-EPMC6143624 | biostudies-literature
Project description:Compensatory growth (CG) is a means by which organisms can increase their growth rate above their routine growth rate after a period of environmentally induced growth depression. Despite a focus on the implications of CG for aquaculture, little research has evaluated the effect of domesticated-wild hybridization on CG. Any deviation in the mean compensatory ability of hybrids relative to their wild progenitors, or any notable costs to compensation in terms of body morphology, could affect the ability of hybrids to persist in changing environments. We compared CG of farmed, wild and hybrid (F1, F2, wild backcross) juvenile Atlantic salmon (Salmo salar). Wild salmon experienced both lower routine and CG rates relative to farmed salmon, while hybrids were intermediate. However, the compensatory responses (slopes of the reaction norms) for each cross were parallel, indicating that hybridization did not affect the CG response itself. Morphological costs to compensation were not detected. In addition to contributing to risk assessments of the consequences of interbreeding between wild and escaped domesticated organisms, we conclude that plasticity studies on domesticated-wild hybrids and their progenitors are useful for testing basic predictions about the evolution of phenotypic plasticity, as well as understanding the evolutionary significance of hybrids.
| S-EPMC3352526 | biostudies-literature
Project description:Salmon have been widely publicized as a good dietary source of vitamin D, but recent data points to large variation in vitamin D content and differences between wild and farmed salmon. We aimed to: (1) investigate the content of vitamin D in Atlantic salmon (Salmo salar) in wild species caught in two different waters, (2) perform a 12-week feeding trial in farmed Salmo salar with 270-1440 µg vitamin D3/kg feed (4-20 times maximum level in the EU) and (3) conduct a review for the published data on the content of vitamin D in salmonids. Content of vitamin D3 in the fillet from wild salmon caught in the Baltic Sea and the North Sea was significantly different (p < 0.05), being 18.5 ± 4.6 µg/100 g and 9.4 ± 1.9 µg/100 g, respectively. In the farmed salmon the content ranged from 2.9 ± 0.7 µg vitamin D3/100 g to 9.5 ± 0.7 µg vitamin D3/100 g. Data from 2018 shows that farmed salmon contained 2.3-7.3 µg vitamin D3/100 g. Information on the content of vitamin D in wild and farmed salmonids is very limited, which calls for further research to ensure a sustainable production of salmon with adequate vitamin D.
| S-EPMC6566758 | biostudies-literature