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Estimates of Natural Selection in a Salmon Population in Captive and Natural Environments

Conservation Biology Division, Northwest Fisheries Science Center, 2725 Montlake Boulevard E. Seattle, WA 98112, USA.
Conservation Biology (Impact Factor: 4.32). 07/2008; 22(3):783-94. DOI: 10.1111/j.1523-1739.2008.00965.x
Source: PubMed

ABSTRACT Captive breeding is a commonly used strategy for species conservation. One risk of captive breeding is domestication selection--selection for traits that are advantageous in captivity but deleterious in the wild. Domestication selection is of particular concern for species that are bred in captivity for many generations and that have a high potential to interbreed with wild populations. Domestication is understood conceptually at a broad level, but relatively little is known about how natural selection differs empirically between wild and captive environments. We used genetic parentage analysis to measure natural selection on time of migration, weight, and morphology for a coho salmon (Oncorhynchus kisutch) population that was subdivided into captive and natural components. Our goal was to determine whether natural selection acting on the traits we measured differed significantly between the captive and natural environments. For males, larger individuals were favored in both the captive and natural environments in all years of the study, indicating that selection on these traits in captivity was similar to that in the wild. For females, selection on weight was significantly stronger in the natural environment than in the captive environment in 1 year and similar in the 2 environments in 2 other years. In both environments, there was evidence of selection for later time of return for both males and females. Selection on measured traits other than weight and run timing was relatively weak. Our results are a concrete example of how estimates of natural selection during captivity can be used to evaluate this common risk of captive breeding programs.

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    • "While the first step in the process has been successfully accomplished, as eggs taken from Devils Hole have been hatched in captivity, serious obstacles remain before releases of pupfish can occur. Unfortunately, the longer that pupfish remain in captivity before being returned to the wild, the greater the likelihood of selection for domestication and loss of behaviors needed to survive in the wild (Ford et al., 2008; Frankham, 2008; Kelley, Magurran & Macías García, 2006; Snyder et al., 1996). Avoidance of domestication will be a key priority in managing the captive population (LH Simons, pers. "
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    ABSTRACT: The Devils Hole pupfish is restricted to one wild population in a single aquifer-fed thermal pool in the Desert National Wildlife Refuge Complex. Since 1995 the pupfish has been in a nearly steady decline, where it was perched on the brink of extinction at 35-68 fish in 2013. A major strategy for conserving the pupfish has been the establishment of additional captive or "refuge" populations, but all ended in failure. In 2013 a new captive propagation facility designed specifically to breed pupfish was opened. I examine how a captive population can be initiated by removing fish from the wild without unduly accelerating extinction risk for the pupfish in Devils Hole. I construct a count-based PVA model, parameterized from estimates of the intrinsic rate of increase and its variance using counts in spring and fall from 1995-2013, to produce the first risk assessment for the pupfish. Median time to extinction was 26 and 27 years from spring and fall counts, respectively, and the probability of extinction in 20 years was 26-33%. Removing individuals in the fall had less risk to the wild population than harvest in spring. For both spring and fall harvest, risk increased rapidly when levels exceeded six adult pupfish per year for three years. Extinction risk was unaffected by the apportionment of total harvest among years. A demographic model was used to examine how removal of different stage classes affects the dynamics of the wild population based on reproductive value (RV) and elasticity. Removing eggs had the least impact on the pupfish in Devils Hole; RV of an adult was roughly 25 times that of an egg. To evaluate when it might be prudent to remove all pupfish from Devils Hole for captive breeding, I used the count-based model to examine how extinction risk related to pupfish population size. Risk accelerated when initial populations were less than 30 individuals. Results are discussed in relation to the challenges facing pupfish recovery compared to management of other highly endangered species.
    PeerJ 09/2014; 2(1):e549. DOI:10.7717/peerj.549 · 2.10 Impact Factor
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    • "Artificially reared organisms are thus subject to adaptation to captivity (i.e. domestication selection; Frankham et al. 2002; Ford et al. 2008). Large-scale, human-mediated releases of plants and animals occur worldwide, and when artificially reared individuals are released to the wild, there can be negative genetic effects on native or wild populations (reviewed in Laikre et al. 2010). "
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    ABSTRACT: While supportive breeding programmes strive to minimize negative genetic impacts to populations, case studies have found evidence for reduced fitness of artificially produced individuals when they reproduce in the wild. Pedigrees of two complete generations were tracked with molecular markers to investigate differences in reproductive success (RS) of wild and hatchery-reared Chinook salmon spawning in the natural environment to address questions regarding the demographic and genetic impacts of supplementation to a natural population. Results show a demographic boost to the population from supplementation. On average, fish taken into the hatchery produced 4.7 times more adult offspring, and 1.3 times more adult grand-offspring than naturally reproducing fish. Of the wild and hatchery fish that successfully reproduced, we found no significant differences in RS between any comparisons, but hatchery-reared males typically had lower RS values than wild males. Mean relative reproductive success (RRS) for hatchery F(1) females and males was 1.11 (P = 0.84) and 0.89 (P = 0.56), respectively. RRS of hatchery-reared fish (H) that mated in the wild with either hatchery or wild-origin (W) fish was generally equivalent to W × W matings. Mean RRS of H × W and H × H matings was 1.07 (P = 0.92) and 0.94 (P = 0.95), respectively. We conclude that fish chosen for hatchery rearing did not have a detectable negative impact on the fitness of wild fish by mating with them for a single generation. Results suggest that supplementation following similar management practices (e.g. 100% local, wild-origin brood stock) can successfully boost population size with minimal impacts on the fitness of salmon in the wild.
    Molecular Ecology 10/2012; 21(21):5236-50. DOI:10.1111/mec.12046 · 5.84 Impact Factor
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    • "We also compared selection on body size with a simple length-based egg production model to evaluate the importance of breeding competition amongst females. Finally, to test the hypothesis that selection is strong during colonization , we compared our selection gradients with others in a comprehensive review of selection in natural populations (Kingsolver et al. 2001) and similar salmonid studies (Seamons et al. 2007; Ford et al. 2008). "
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    ABSTRACT: Selection during the colonization of new habitat is critical to the process of local adaptation, but has rarely been studied. We measured the form, direction, and strength of selection on body size and date of arrival to the breeding grounds over the first three cohorts (2003-2005) of a coho salmon (Oncorhynchus kisutch) population colonizing 33 km of habitat made accessible by modification of Landsburg Diversion Dam, on the Cedar River, Washington, USA. Salmon were sampled as they bypassed the dam, parentage was assigned based on genotypes from 10 microsatellite loci, and standardized selection gradients were calculated using the number of returning adult offspring as the fitness metric. Larger fish in both sexes produced more adult offspring, and the magnitude of the effect increased in subsequent years for males, suggesting that low densities attenuated traditional size-biased intrasexual competition. For both sexes, directional selection favoured early breeders in 2003, but stabilizing selection on breeding date was observed in 2004 and 2005. Adults that arrived, and presumably bred, early produced stream-rearing juvenile offspring that were larger at a common date than offspring from later parents, providing a possible mechanism linking breeding date to offspring viability. Comparison to studies employing similar methodology indicated selection during colonization was strong, particularly with respect to reproductive timing. Finally, female mean reproductive success exceeded that needed for replacement in all years so the population expanded in the first generation, demonstrating that salmon can proficiently exploit vacant habitat.
    Molecular Ecology 06/2010; 19(12):2562-73. DOI:10.1111/j.1365-294X.2010.04652.x · 5.84 Impact Factor
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