Cryptic introgression: evidence that selection and plasticity mask the full phenotypic potential of domesticated Atlantic salmon in the wild

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.publishedVersio

Domestication leads to increased predation susceptibilit

Domestication involves adapting animals to the human-controlled environment. Genetic changes occurring during the domestication process may manifest themselves in phenotypes that render domesticated animals maladaptive for life in the wild. Domesticated Atlantic salmon frequently interbreed with wild conspecifics, and their offspring display reduced survival in the wild. However, the mechanism(s) contributing to their lower survival in the wild remains a subject of conjecture. Here, we document higher susceptibility to predation by brown trout in fast-growing domesticated salmon, as compared to their slow-growing wild conspecifics, demonstrating that directional selection for increased growth comes at a cost of decreased survival when under the risk of predation, as predicted by the growth/predation risk trade-off. Despite earlier documentation of altered risk-taking behavior, this study demonstrates for the first time that domestication of Atlantic salmon has lead to increased predation susceptibility, and that this consitutes a mechanism underpinning the observed survial differences in the wild.publishedVersio

Genetic variation for upper thermal tolerance diminishes within and between populations with increasing acclimation temperature in Atlantic salmon

Populations may counteract lasting temperature changes or recurrent extremes through plasticity or adaptation. However, it remains underexplored how outbreeding, either naturally, unintentionally, or facilitated, may modify a local response potential and whether genotype-by-environment interactions or between-trait correlations can restrict this potential. We quantified population differences and outbreeding effects, within-population genetic variation, and plasticity of these, for thermal performance proxy traits using 32 pedigreed wild, domesticated, and wild-domesticated Atlantic salmon families reared under common-garden conditions. Following exposure to ambient cold (11.6 °C) or ~4° and ~8° warmer summer temperatures, populations differed notably for body length and critical thermal maximum (CTmax) and for thermal plasticity of length, condition, and CTmax, but not for haematocrit. Line-cross analysis suggested mostly additive and some dominant outbreeding effects on means and solely additive outbreeding effects on plasticity. Heritability was detected for all traits. However, with increasing acclimation temperature, differences in CTmax between populations and CTmax heritability diminished, and CTmax breeding values re-ranked. Furthermore, CTmax and body size were negatively correlated at the genetic and phenotypic levels, and there was indirect evidence for a positive correlation between growth potential and thermal performance breadth for growth. Thus, population differences (including those between wild and domesticated populations) in thermal performance and plasticity may present a genetic resource in addition to the within-population genetic variance to facilitate, or impede, thermal adaptation. However, unfavourable genotype-by-environment interactions and negative between-trait correlations may generally hamper joint evolution in response to an increase in average temperature and temporary extremes.publishedVersio

Morphological consequences of hybridization between farm and wild Atlantic salmon Salmo salar under both wild and experimental conditions

The escape of Atlantic salmon Salmo salar from aquaculture has been identified as a significant threat to the persistence and stability of wild salmon populations. Yet the magnitude of phenotypic impacts due to hybridization remains largely unresolved. We evaluated the phenotypic consequences of hybridization using geometric morphometrics both under natural conditions in the wild and in the laboratory using common garden experiments. Juvenile Atlantic salmon field-collected in 2015 and 2016 from 18 southern Newfoundland rivers were classified as pure wild, pure farm, or F1 hybrids using genetic assignment. Overall size and shape differences between wild and farm, and wild and F1 hybrid individuals were small, largely size related, and present between pure farm and other crosses. Laboratory-reared pure wild, pure farm, and F1 hybrid salmon were grown in tank and semi-natural conditions. Wild fish were significantly larger than both farm and hybrid salmon at first feeding; these size differences remained at 80 d post first feeding under semi-natural conditions, but all crosses were the same size in tank conditions, and there were no differences between pure farm and hybrid individuals under either condition. Significant shape differences were present among all pairwise comparisons under tank conditions, and in semi-natural conditions, pure wild individuals differed significantly from pure farm and hybrid individuals. Our results suggest phenotypic differences observed under laboratory conditions between wild and farm×wild hybrid individuals may not be appreciable in the wild, and that significant genetic changes may occur in wild populations experiencing hybridization in the absence of obvious large phenotypic changes.publishedVersio

Introgression of domesticated salmon changes life history and phenology of a wild salmon population

The release of domesticated conspecifics into the natural environment, whether deliberate or accidental, has the potential to alter the genetic integrity and evolutionary trajectory of wild populations. This widespread challenge is of particular concern for wild Atlantic salmon. By investigating phenotypic differences between the offspring of domesticated, hybrid, and wild Atlantic salmon released into the natural environment, earlier studies have documented the short-term consequences of introgression from domesticated fish into wild salmon populations. However, few studies have investigated the joined product of introgression and natural selection after several generations. Here, we investigated the phenotypic response of an Atlantic salmon population that has been subjected to an average of 24% genetic admixture by domesticated conspecifics escaping from fish farms over three decades (approximately 6–7 generations). Individual levels of admixture were positively correlated with increased size at the smolt and adult stages for both sexes, a decrease in the age of male smolts, and a decrease in the age at maturity for males. These life history changes are presumably the consequence of the well-documented directional selection for increased growth in domesticated salmon and are likely maladaptive. However, the most novel result of this study is that admixture was positively linked with delayed date of return to the river, with highly admixed fish arriving up to 26 days later than nonadmixed fish. Potentially, this phenological change provides admixed individuals with a survival advantage in the later phase of the life cycle as it reduces their period of exposure to selection through rod and line angling. We, therefore, conclude that while gene flow from domesticated conspecifics changes life history and phenological traits of wild Atlantic salmon populations, most of which are likely to be maladaptive, when pressured by additional anthropogenic challenges, some changes may confer a fitness advantage for a short part of the life cycle.publishedVersio

Red and melanized focal changes in white skeletal muscle in Atlantic salmon (Salmo salar): Comparative analysis of farmed, wild and hybrid fish reared under identical conditions

Selective breeding plays a vital role in the production of farmed Atlantic salmon and has shown success in many aspects. Still, challenges related to fish health and welfare continue to result in significant economic losses. One such challenge is red and melanized focal changes (RFC/MFC), which result from acute and chronic inflammation, respectively, in the skeletal muscle. Importantly, RFC/MFC has not been observed in wild Atlantic salmon, suggesting that both external and genetic factors may contribute to the development of inflammation. To investigate the underlying cause of RFC/MFC, we conducted a study involving 1854 Atlantic salmon of farmed, wild and hybrid origin. All fish were reared under identical conditions to minimize the influence of external factors. Throughout the production cycle, the fish was monitored for growth parameters and examined for RFC/MFC using macroscopic and histological analysis. We found no association between the experimental groups and the presence of RFC/MFC. Histological investigations revealed melano-macrophages in the soft tissue in freshwater smolt, although no macroscopic discoloration was observed. MFC showed granulomas in various stages, suggesting a complex progression of the condition. In summary, we conclude that RFC/MFC is primarily caused by external factors found in the rearing facilities of farmed Atlantic salmon.publishedVersio

The influence of vgll3 genotypes on sea age at maturity is altered in farmed mowi strain Atlantic salmon

Background: In Atlantic salmon in the wild, age at maturity is strongly influenced by the vgll3 locus. Under farming conditions, light, temperature and feeding regimes are known significantly advance or delay age at maturity. However, the potential influence of the vgll3 locus on the maturation of salmon reared under farming conditions has been rarely investigated, especially in females. Results: Here, we reared domesticated salmon (mowi strain) with different vgll3 genotypes under standard farming conditions until they matured at either one, two or more than two sea winters. Interestingly, and in contrast to previous findings in the wild, we were not able to identify a link between vgll3 and age at maturity in females when reared under farming conditions. For males however, we found that the probability of delaying maturation from one to two sea winters was significantly lower in fish homozygous for the early allele compared to homozygous fish for the late allele, while the probability for heterozygous fish was intermediate. These data also contrast to previous findings in the wild where the early allele has been reported as dominant. However, we found that the probability of males delaying maturation from two to three sea winters was regulated in the same manner as the wild. Conclusions: Collectively, our data suggest that increased growth rates in mowi salmon, caused by high feed intake and artificial light and temperature regimes together with other possible genetic/epigenetic components, may significantly influence the impact that the vgll3 locus has on age at maturity, especially in females. In turn, our results show that the vgll3 locus can only to a large extent be used in selective breeding to control age at maturation in mowi males. In summary, we here show that in contrast to the situation in wild salmon, under farming conditions vgll3 does not seem to influence age at maturity in mowi females whereas in mowi males, maturing as one or two sea winters it alters the early allele effect from dominant to intermediatepublishedVersio

Plasticity in growth of farmed and wild Atlantic salmon:Is the increased growth rate of farmed salmon caused by evolutionary adaptations to the commercial diet?

Background: Domestication of Atlantic salmon for commercial aquaculture has resulted in farmed salmon displaying substantially higher growth rates than wild salmon under farming conditions. In contrast, growth differences between farmed and wild salmon are much smaller when compared in the wild. The mechanisms underlying this contrast between environments remain largely unknown. It is possible that farmed salmon have adapted to the high-energy pellets developed specifically for aquaculture, contributing to inflated growth differences when fed on this diet. We studied growth and survival of 15 families of farmed, wild and F1 hybrid salmon fed three contrasting diets under hatchery conditions; a commercial salmon pellet diet, a commercial carp pellet diet, and a mixed natural diet consisting of preserved invertebrates commonly found in Norwegian rivers.  Results: For all groups, despite equal numbers of calories presented by all diets, overall growth reductions as high 68 and 83%, relative to the salmon diet was observed in the carp and natural diet treatments, respectively. Farmed salmon outgrew hybrid (intermediate) and wild salmon in all treatments. The relative growth difference between wild and farmed fish was highest in the carp diet (1: 2.1), intermediate in the salmon diet (1:1.9) and lowest in the natural diet (1:1.6). However, this trend was non-significant, and all groups displayed similar growth reaction norms and plasticity towards differing diets across the treatments.  Conclusions: No indication of genetic-based adaptation to the form or nutritional content of commercial salmon diets was detected in the farmed salmon. Therefore, we conclude that diet alone, at least in the absence of other environmental stressors, is not the primary cause for the large contrast in growth differences between farmed and wild salmon in the hatchery and wild. Additionally, we conclude that genetically-increased appetite is likely to be the primary reason why farmed salmon display higher growth rates than wild salmon when fed ad lib rations under hatchery conditions. Our results contribute towards an understanding of the potential genetic changes that have occurred in farmed salmon in response to domestication, and the potential mechanisms underpinning genetic and ecological interactions between farmed escapees and wild salmonids

The future looks like the past: Introgression of domesticated Atlantic salmon escapees in a risk assessment framework

Escapes of domesticated fish from aquaculture, followed by interbreeding with wild conspecifics, represent a threat to the genetic integrity and evolutionary trajectory of natural populations. Approximately fifty years of Atlantic salmon production has left an unprecedented legacy of widespread introgression of domesticated escapees in wild Norwegian populations. A major question, however, is whether current aquaculture practice will lead to additional introgression in the near future. As part of the updated Norwegian risk assessment of fish farming, we conducted a risk assessment for further introgression of domesticated escapees in wild populations in Norway. Extensive data of reported numbers of escapees, observed proportions of escapees in rivers, removal of escapees pre‐spawning, and the resilience of wild populations through demographic and genetic status informed the risk assessment. The analysis revealed that rivers in 10 of the 13 aquaculture production zones covering Norway display a moderate or high risk of further introgression of domesticated escapees. This comes in addition to widespread introgression that is already documented. We therefore conclude that so long as aquaculture production continues at its present level and form, there is a moderate‐to‐high risk of further introgression of domesticated salmon in many native populations throughout much of Norway.publishedVersio