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

ABSTRACT: 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.

SUBMITTER: Glover KA

PROVIDER: S-EPMC6143624 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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

Glover Kevin A KA Solberg Monica F MF Besnier Francois F Skaala Øystein Ø

Scientific reports 20180918 1

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 sal ...[more]

PMID: 30228303

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Project description: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.

Project description:BACKGROUND:Mature male parr (MMP) represent an important alternative life-history strategy in Atlantic salmon populations. Previous studies indicate that the maturation size threshold for male parr varies among wild populations and is influenced by individual growth, environmental conditions, and genetics. More than ten generations of breeding have resulted in domesticated salmon displaying many genetic differences to wild salmon, including greatly increased growth rates. This may have resulted in domesticated fish with the potential to outgrow the size threshold for early maturation, or evolution of the size threshold of the trait itself. To investigate this, we performed a common-garden experiment under farming conditions using 4680 salmon from 39 families representing four wild, two wild-domesticated hybrid, and two domesticated strains. RESULTS:Domesticated salmon outgrew wild salmon 2-5-fold, and hybrids displayed intermediate growth. Overall, the numbers of MMP varied greatly among families and strains: averaging 4-12% in domesticated, 18-25% in hybrid, and 43-74% in the wild populations. However, when the influence of growth was accounted for, by dividing fish into lower and upper size modes, no difference in the incidence of MMP was detected among domesticated and wild strains in either size mode. In the lower size mode, hybrids displayed significantly lower incidences of mature males than their wild parental strains. No consistent differences in the body size of MMP, connected to domestication, was detected. CONCLUSIONS:Our data demonstrate: 1- no evidence for the evolution of the size threshold for MMP in domesticated salmon, 2- the vastly lower incidence of MMP in domesticated strains under aquaculture conditions is primarily due to their genetically increased growth rate causing them to outgrow the size threshold for early maturation, 3- the incidence of MMP is likely to overlap among domesticated and wild salmon in the natural habitat where they typically display overlapping growth, although hybrid offspring may display lower incidences of mature male parr. These results have implications for wild salmon populations that are exposed to introgression from domesticated escapees.

Project description:BackgroundDomestication is the process by which organisms become adapted to the human-controlled environment. Since the selection pressures that act upon cultured and natural populations differ, adaptations that favour life in the domesticated environment are unlikely to be advantageous in the wild. Elucidation of the differences between wild and domesticated Atlantic salmon may provide insights into some of the genomic changes occurring during domestication, and, help to predict the evolutionary consequences of farmed salmon escapees interbreeding with wild conspecifics. In this study the transcriptome of the offspring of wild and domesticated Atlantic salmon were compared using a common-garden experiment under standard hatchery conditions and in response to an applied crowding stressor.ResultsTranscriptomic differences between wild and domesticated crosses were largely consistent between the control and stress conditions, and included down-regulation of environmental information processing, immune and nervous system pathways and up-regulation of genetic information processing, carbohydrate metabolism, lipid metabolism and digestive and endocrine system pathways in the domesticated fish relative to their wild counterparts, likely reflective of different selection pressures acting in wild and cultured populations. Many stress responsive functions were also shared between crosses and included down-regulation of cellular processes and genetic information processing and up-regulation of some metabolic pathways, lipid and energy in particular. The latter may be indicative of mobilization and reallocation of energy resources in response to stress. However, functional analysis indicated that a number of pathways behave differently between domesticated and wild salmon in response to stress. Reciprocal F1 hybrids permitted investigation of inheritance patterns that govern transcriptomic differences between these genetically divergent crosses. Additivity and maternal dominance accounted for approximately 42 and 25% of all differences under control conditions for both hybrids respectively. However, the inheritance of genes differentially expressed between crosses under stress was less consistent between reciprocal hybrids, potentially reflecting maternal environmental effects.ConclusionWe conclude that there are transcriptomic differences between the domesticated and wild salmon strains studied here, reflecting the different selection pressures operating on them. Our results indicate that stress may affect certain biological functions differently in wild, domesticated and hybrid crosses and these should be further investigated.

Project description:BACKGROUND:Directional selection for growth has resulted in the 9-10th generation of domesticated Atlantic salmon Salmo salar L. outgrowing wild salmon by a ratio of approximately 3:1 when reared under standard hatchery conditions. In the wild however, growth of domesticated and wild salmon is more similar, and seems to differ at the most by a ratio of 1.25:1. Comparative studies of quantitative traits in farmed and wild salmon are often performed by the use of common-garden experiments where salmon of all origins are reared together to avoid origin-specific environmental differences. As social interaction may influence growth, the large observed difference in growth between wild and domesticated salmon in the hatchery may not be entirely genetically based, but inflated by inter-strain competition. This study had two primary aims: (i) investigate the effect of social interaction and inter-strain competition in common-garden experiments, by comparing the relative growth of farmed, hybrid and wild salmon when reared together and separately; (ii) investigate the competitive balance between wild and farmed salmon by comparing their norm of reaction for survival and growth along an environmental gradient ranging from standard hatchery conditions to a semi-natural environment with restricted feed. RESULTS:The main results of this study, which are based upon the analysis of more than 6000 juvenile salmon, can be summarised as; (i) there was no difference in relative growth between wild and farmed salmon when reared together and separately; (ii) the relative difference in body weight at termination between wild and farmed salmon decreased as mortality increased along the environmental gradient approaching natural conditions. CONCLUSIONS:This study demonstrates that potential social interactions between wild and farmed salmon when reared communally are not likely to cause an overestimation of the genetic growth differences between them. Therefore, common-garden experiments represent a valid methodological approach to investigate genetic differences between wild and farmed salmon. As growth of surviving salmon of all origins became more similar as mortality increased along the environmental gradient approaching natural conditions, a hypothesis is presented suggesting that size-selective mortality is a possible factor reducing growth differences between these groups in the wild.

Project description:Interactions between domesticated escapees and wild conspecifics represent a threat to the genetic integrity and fitness of native populations. For Atlantic salmon, the recurrent presence of large numbers of domesticated escapees in the wild makes it necessary to better understand their impacts on native populations. We planted 254,400 eggs from 75 families of domesticated, F1-hybrid, and wild salmon in a river containing up- and downstream traps. Additionally, 41,630 hatchery smolts of the same pedigrees were released into the river. Over 8 years, 6,669 out-migrating smolts and 356 returning adults were recaptured and identified to their families of origin with DNA. In comparison with wild salmon, domesticated fish had substantially lower egg to smolt survival (1.8% vs. 3.8% across cohorts), they migrated earlier in the year (11.8 days earlier across years), but they only displayed marginally larger smolt sizes and marginally lower smolt ages. Upon return to freshwater, domesticated salmon were substantially larger at age than wild salmon (2.4 vs. 2.0, 4.8 vs. 3.2, and 8.5 vs. 5.6 kg across sexes for 1, 2, and 3 sea-winter fish) and displayed substantially lower released smolt to adult survival (0.41% vs. 0.94% across releases). Overall, egg-to-returning adult survival ratios were 1:0.76:0.30 and 1:0.44:0.21 for wild:F1-hybrid:domesticated salmon, respectively, using two different types of data. This study represents the most updated and extensive analysis of domesticated, hybrid, and wild salmon in the wild and provides the first documentation of a clear genetic difference in the timing of smolt migration-an adaptive trait presumed to be linked with optimal timing of entry to seawater. We conclude that spawning and hybridization of domesticated escapees can lead to (i) reduced wild smolt output and therefore wild adult abundance, through resource competition in freshwater, (ii) reduced total adult abundance due to freshwater competition and reduced marine survival of domesticated salmon, and (iii) maladaptive changes in phenotypic traits.

Dataset Information

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

Publications

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

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