Captive breeding programs are widely used for the conservation and restoration of threatened and endangered species. Nevertheless, captive-born individuals frequently have reduced fitness when reintroduced into the wild. The mechanism for these fitness declines has remained elusive, but hypotheses include environmental effects of captive rearing, inbreeding among close relatives, relaxed natural selection, and unintentional domestication selection (adaptation to captivity). We used a multigenerational pedigree analysis to demonstrate that domestication selection can explain the precipitous decline in fitness observed in hatchery steelhead released into the Hood River in Oregon. After returning from the ocean, wild-born and first-generation hatchery fish were used as broodstock in the hatchery, and their offspring were released into the wild as smolts. First-generation hatchery fish had nearly double the lifetime reproductive success (measured as the number of returning adult offspring) when spawned in captivity compared with wild fish spawned under identical conditions, which is a clear demonstration of adaptation to captivity. We also documented a tradeoff among the wild-born broodstock: Those with the greatest fitness in a captive environment produced offspring that performed the worst in the wild. Specifically, captive-born individuals with five (the median) or more returning siblings (i.e., offspring of successful broodstock) averaged 0.62 returning offspring in the wild, whereas captive-born individuals with less than five siblings averaged 2.05 returning offspring in the wild. These results demonstrate that a single generation in captivity can result in a substantial response to selection on traits that are beneficial in captivity but severely maladaptive in the wild.fisheries | genetics | parentage | rapid evolution | salmon C aptive breeding programs are commonly used for the conservation of endangered species and, more recently, for the restoration of declining populations (1-4). Mounting evidence suggests that captive-born individuals released into the wild can have substantially lower fitness than their wild-born counterparts and that these fitness declines can occur after only a few generations in captivity (5-8). Identifying the mechanisms that cause reduced fitness in the wild is vital for deciding if, when, and how captive breeding programs should be applied for conservation and management purposes (5, 7). Explanations for the rapid fitness declines (8-12) include environmental effects of captive rearing (including heritable epigenetic effects), inbreeding among close relatives, relaxed natural selection, and unintentional domestication selection (adaptation to the novel environment). Each of these mechanisms creates subtle but testable differences in patterns of reproductive success.Environmental effects of captive rearing, for example, could produce differences in fitness between captive-born and wildborn individuals but would not create differences in fitness among individuals that experienced ...
Large numbers of hatchery salmon spawn in wild populations each year. Hatchery fish with multiple generations of hatchery ancestry often have heritably lower reproductive success than wild fish and may reduce the fitness of an entire population. Whether this reduced fitness also occurs for hatchery fish created with local- and predominantly wild-origin parents remains controversial. Here, we review recent studies on the reproductive success of such ‘early-generation’ hatchery fish that spawn in the wild. Combining 51 estimates from six studies on four salmon species, we found that (i) early-generation hatchery fish averaged only half the reproductive success of their wild-origin counterparts when spawning in the wild, (ii) the reduction in reproductive success was more severe for males than for females, and (iii) all species showed reduced fitness due to hatchery rearing. We review commonalities among studies that point to possible mechanisms (e.g., environmental versus genetic effects). Furthermore, we illustrate that sample sizes typical of these studies result in low statistical power to detect fitness differences unless the differences are substantial. This review demonstrates that reduced fitness of early-generation hatchery fish may be a general phenomenon. Future research should focus on determining the causes of those fitness reductions and whether they lead to long-term reductions in the fitness of wild populations.
Identifying patterns of larval dispersal within marine metapopulations is vital for effective fisheries management, appropriate marine reserve design, and conservation efforts. We employed genetic markers (microsatellites) to determine dispersal patterns in bicolour damselfish (Pomacentridae: Stegastes partitus). Tissue samples of 751 fish were collected in 2004 and 2005 from 11 sites encompassing the Exuma Sound, Bahamas. Bayesian parentage analysis identified two parent-offspring pairs, which is remarkable given the large population sizes and 28 day pelagic larval duration of bicolour damselfish. The two parent-offspring pairs directly documented self-recruitment at the two northern-most sites, one of which is a long-established marine reserve. Principal coordinates analyses of pair-wise relatedness values further indicated that self-recruitment was common in all sampled populations. Nevertheless, measures of genetic differentiation (F ST ) and results from assignment methods suggested high levels of gene flow among populations. Comparisons of heterozygosity and relatedness among samples of adults and recruits indicated spatially and temporally independent sweepstakes events, whereby only a subset of adults successfully contribute to subsequent generations. These results indicate that self-recruitment and sweepstakes reproduction are the predominant, ecologically-relevant processes that shape patterns of larval dispersal in this system.
The genetic underpinnings associated with the earliest stages of plant and animal domestication have remained elusive. Because a genome-wide response to selection can take many generations, the earliest detectable changes associated with domestication may first manifest as heritable changes to global patterns of gene expression. Here, to test this hypothesis, we measured differential gene expression in the offspring of wild and first-generation hatchery steelhead trout (Oncorhynchus mykiss) reared in a common environment. Remarkably, we find that there were 723 genes differentially expressed between the two groups of offspring. Reciprocal crosses reveal that the differentially expressed genes could not be explained by maternal effects or by chance differences in the background levels of gene expression among unrelated families. Gene-enrichment analyses reveal that adaptation to the novel hatchery environment involved responses in wound healing, immunity and metabolism. These findings suggest that the earliest stages of domestication may involve adaptation to highly crowded conditions.
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