Gene flow from domesticated escapes alters the life history of wild Atlantic salmon

Bolstad, Geir H.; Hindar, Kjetil; Robertsen, Grethe; Jönsson, Bror; Sægrov, Harald; Diserud, Ola Håvard; Fiske, Peder; Jensen, Arne J.; Urdal, Kurt; Næsje, Tor F.; Barlaup, Bjørn Torgeir; Florø-Larsen, Bjørn; Lo, Håvard; Niemelä, Eero; Karlsson, Sten

doi:10.1038/s41559-017-0124

Cited by 118 publications

(130 citation statements)

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“…This is, however, in line with the previously reported finding that phenotypic F I G U R E 4 Estimated relationship between individual mass (g, lntransformed) of Atlantic salmon juveniles in semi-natural stream channels at the termination of the experiment and (a) family-level embryo mass (g, lntransformed), and (b) number of surviving juveniles in each stream channel plotted on raw data effects of farmed introgression vary among wild Atlantic salmon populations (Bolstad et al, 2017). Embryos of farmed males had significantly higher SMR than embryos of wild males in the crosses between farmed salmon and wild salmon of the Imsa population, but there was not a similar finding in the Surna population.…”

Section: Discussionsupporting

confidence: 87%

Can variation in standard metabolic rate explain context‐dependent performance of farmed Atlantic salmon offspring?

Robertsen

Reid

Einum

et al. 2018

Ecology and Evolution

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Escaped farmed Atlantic salmon interbreed with wild Atlantic salmon, leaving offspring that often have lower success in nature than pure wild salmon. On top of this, presence of farmed salmon descendants can impair production of wild‐type recruits. We hypothesize that both these effects connect with farmed salmon having acquired higher standard metabolic rates (SMR, the energetic cost of self‐maintenance) during domestication. Fitness‐related advantages of phenotypic traits associated with both high SMR and farmed salmon (e.g., social dominance) depend on environmental conditions, such as food availability. We hypothesize that farmed offspring have an advantage at high food availability due to, for example, dominance behavior but suffer increased risks of starvation when food is scarce because this behavior is energy‐demanding. To test these hypotheses, we first compare embryo SMR of pure farmed, farmed‐wild hybrids and pure wild offspring. Next, we test early‐life performance (in terms of survival and growth) of hybrids relative to that of their wild half‐siblings, as well as their competitive abilities, in semi‐natural conditions of high and low food availability. Finally, we test how SMR affects early‐life performance at high and low food availability. We find inconclusive support for the hypothesis that domestication has induced increased SMR. Further, wild and hybrid juveniles had similar survival and growth in the semi‐natural streams. Yet, the presence of hybrids led to decreased survival of their wild half‐siblings. Contrary to our hypothesis about context‐dependency, these effects were not modified by food availability. However, wild juveniles with high SMR had decreased survival when food was scarce, but there was no such effect at high food availability. This study provides further proof that farmed salmon introgression may compromise the viability of wild salmon populations. We cannot, however, conclude that this is connected to alterations in the metabolic phenotype of farmed salmon.

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Section: Discussionsupporting

confidence: 87%

Can variation in standard metabolic rate explain context‐dependent performance of farmed Atlantic salmon offspring?

Robertsen

Reid

Einum

et al. 2018

Ecology and Evolution

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“…Others have concluded that growth differences between domesticated, hybrid, and wild salmon in the marine phase are not necessarily very clear, with small differences in maximum size at age but significant differences in minimum size at age (Jonsson & Jonsson, ). While the response in adult size in the IBSEM outputs reported here is low in comparison with the observations between domestication‐admixed and nonadmixed salmon (Figure vs. results by Bolstad et al., ), it is pertinent to point out that the model outputs here reflect the population average. We did not separate out domestication‐admixed and nonadmixed fish as was the case in the analysis by Bolstad and colleagues (Bolstad et al., ).…”

Section: Discussioncontrasting

confidence: 77%

“…While the response in adult size in the IBSEM outputs reported here is low in comparison with the observations between domestication‐admixed and nonadmixed salmon (Figure vs. results by Bolstad et al., ), it is pertinent to point out that the model outputs here reflect the population average. We did not separate out domestication‐admixed and nonadmixed fish as was the case in the analysis by Bolstad and colleagues (Bolstad et al., ). It is therefore suggested that the response revealed here is not necessarily very different to the observations made by Bolstad and colleagues, although this requires further investigation.…”

Section: Discussioncontrasting

confidence: 77%

“…Field experiments have demonstrated that the offspring of domesticated salmon, and hybrids between domesticated and wild salmon, display reduced survival in the wild when compared to the offspring of pure wild salmon (Fleming et al., ; McGinnity et al., , ; Skaala et al., ). Furthermore, differences in phenotypic characteristics such as size at maturation have been reported between admixed and nonadmixed salmon in Norwegian populations where introgression of domesticated fish has occurred (Bolstad et al., ). Nevertheless, in most regions outside Norway where domesticated and wild salmon also overlap, there are almost no estimates of gene‐flow, and the resulting biological consequences have not been investigated (Glover et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Modeling fitness changes in wild Atlantic salmon populations faced by spawning intrusion of domesticated escapees

Castellani

Heino

Gilbey

et al. 2018

Evolutionary Applications

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Genetic interaction between domesticated escapees and wild conspecifics represents a persistent challenge to an environmentally sustainable Atlantic salmon aquaculture industry. We used a recently developed eco‐genetic model (IBSEM) to investigate potential changes in a wild salmon population subject to spawning intrusion from domesticated escapees. At low intrusion levels (5%–10% escapees), phenotypic and demographic characteristics of the recipient wild population only displayed weak changes over 50 years and only at high intrusion levels (30%–50% escapees) were clear changes visible in this period. Our modeling also revealed that genetic changes in phenotypic and demographic characteristics were greater in situations where strayers originating from a neighboring wild population were domestication‐admixed and changed in parallel with the focal wild population, as opposed to nonadmixed. While recovery in the phenotypic and demographic characteristics was observed in many instances after domesticated salmon intrusion was halted, in the most extreme intrusion scenario, the population went extinct. Based upon results from these simulations, together with existing knowledge, we suggest that a combination of reduced spawning success of domesticated escapees, natural selection purging maladapted phenotypes/genotypes from the wild population, and phenotypic plasticity, buffer the rate and magnitude of change in phenotypic and demographic characteristics of wild populations subject to spawning intrusion of domesticated escapees. The results of our simulations also suggest that under specific conditions, natural straying among wild populations may buffer genetic changes in phenotypic and demographic characteristics resulting from introgression of domesticated escapees and that variation in straying in time and space may contribute to observed differences in domestication‐driven introgression among native populations.

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“…; Bolstad et al. ), having perhaps reached some intermediate balance between migration and selection (as in Tufto ) prior to the cessation of introgression, the difference being the initial conditions.…”

Section: Model and Resultsmentioning

confidence: 99%

Domestication and fitness in the wild: A multivariate view

Tufto

2017

Evolution

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Domesticated species continually escaping and interbreeding with wild relatives impose a migration load on wild populations. As domesticated stocks become increasingly different as a result of artificial and natural selection in captivity, fitness of escapees in the wild is expected to decline, reducing the effective rate of migration into wild populations. Recent theory suggest that this may alleviate and eventually eliminate the resulting migration load. I develop a multivariate model of trait and wild fitness evolution resulting from the joint effects of artificial and natural selection in the captive environment. Initially, the evolutionary trajectory is dominated by the effects of artificial selection causing a fast initial decline in fitness of escapees in the wild. In later phases, through the counteracting effects of correlational multivariate natural selection in captivity, the mean phenotype is pushed in directions of weak stabilizing selection, allowing a sustained response in the trait subject to artificial selection. Provided that there is some alignment between the adaptive landscapes in the wild and in captivity, these phases are associated with slower rates of decline in wild fitness of the domesticated stock, suggesting that detrimental effects on wild populations are likely to remain a concern in the foreseeable future.

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Gene flow from domesticated escapes alters the life history of wild Atlantic salmon

Cited by 118 publications

References 50 publications

Can variation in standard metabolic rate explain context‐dependent performance of farmed Atlantic salmon offspring?

Can variation in standard metabolic rate explain context‐dependent performance of farmed Atlantic salmon offspring?

Modeling fitness changes in wild Atlantic salmon populations faced by spawning intrusion of domesticated escapees

Domestication and fitness in the wild: A multivariate view

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