Rapid Evolution of Egg Size in Captive Salmon

Heath, Daniel D.; Heath, John; Bryden, Colleen A; Johnson, Rachel M.; Fox, Charles

doi:10.1126/science.1079707

Cited by 261 publications

(262 citation statements)

References 27 publications

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“…Previous work has suggested that growth rate may be under strong selection in hatcheries because steelhead are released as yearling smolts, whereas fish in the wild generally take 2 y or longer to smolt (22). Other possible contenders for selected traits include egg size, fecundity, physiological processes associated with smoltification, and individual behaviors (e.g., predator avoidance) (10,(22)(23)(24). For the F1 runyear in which selection was not detected (1995), the smolts were reared in low-density conditions and the release size of the smolts was considerably larger than in other years (Table S3), which points to crowding as a possible selection pressure (25).…”

Section: Discussionmentioning

confidence: 99%

Genetic adaptation to captivity can occur in a single generation

Christie

Marine

French

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

368

339

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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 ...

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Section: Discussionmentioning

confidence: 99%

Genetic adaptation to captivity can occur in a single generation

Christie

Marine

French

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

368

339

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“…When maternal effects are themselves heritable, populations can still respond to natural selection via indirect genetic effects [9]. Indeed, in a captive population of chinook salmon, a mother-daughter regression revealed egg mass to be highly heritable, indicative of a genetic basis for egg provisioning [32].…”

Section: Discussionmentioning

confidence: 99%

Indirect genetic effects underlie oxygen-limited thermal tolerance within a coastal population of chinook salmon

et al. 2014

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With global temperatures projected to surpass the limits of thermal tolerance for many species, evaluating the heritable variation underlying thermal tolerance is critical for understanding the potential for adaptation to climate change. We examined the evolutionary potential of thermal tolerance within a population of chinook salmon (Oncorhynchus tshawytscha) by conducting a full-factorial breeding design and measuring the thermal performance of cardiac function and the critical thermal maximum (CT max ) of offspring from each family. Additive genetic variation in offspring phenotype was mostly negligible, although these direct genetic effects explained 53% of the variation in resting heart rate ( f H ). Conversely, maternal effects had a significant influence on resting f H , scope for f H , cardiac arrhythmia temperature and CT max . These maternal effects were associated with egg size, as indicated by strong relationships between the mean egg diameter of mothers and offspring thermal tolerance. Because egg size can be highly heritable in chinook salmon, our finding indicates that the maternal effects of egg size constitute an indirect genetic effect contributing to thermal tolerance. Such indirect genetic effects could accelerate evolutionary responses to the selection imposed by rising temperatures and could contribute to the population-specific thermal tolerance that has recently been uncovered among Pacific salmon populations.

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“…As a result, captive bred animals often have reduced fitness when reintroduced to natural conditions (5). Selective pressures disrupted by captivity include inbreeding avoidance, effective population size, disease exposure, predation, and sexual selection.…”

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confidence: 99%

Reintroducing domesticated wild mice to sociality induces adaptive transgenerational effects on MUP expression

Nelson

Cauceglia

Merkley

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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When brought into captivity, wild animals can adapt to domestication within 10 generations. Such adaptations may decrease fitness in natural conditions. Many selective pressures are disrupted in captivity, including social behavioral networks. Although lack of sociality in captivity appears to mediate domestication, the underlying mechanisms are not well understood. Additionally, determining the contribution of genetic inheritance vs. transgenerational effects during relaxed selection may provide insight into the flexibility of adaptation. When wild-derived mice kept under laboratory conditions for eight generations were reintroduced to sociality and promiscuity (free mate choice), they adapted within two generations. Fitness assessments between this promiscuous lineage and a monogamous laboratory lineage revealed malespecific effects. Promiscuous-line males had deficits in viability, but a striking advantage in attracting mates, and their scent marks were also more attractive to females. Here, we investigate mechanistic details underlying this olfactory signal and identify a role of major urinary protein (MUP) pheromones. Promiscuous-line males inherit higher MUP expression than monogamous-line males through transgenerational inheritance. Sociality-driven maternal and paternal effects reveal intriguing conflicts among parents and offspring over pheromone expression. MUP up-regulation is not driven by hormone-driven transduction pathways, but rather is associated with reduction in DNA methylation of a CpG dinucleotide in the promoter. This reduction in methylation could enhance transcription by promoting the binding of transcription factor USF1 (upstream stimulatory factor 1). Finally, we experimentally demonstrate that increased MUP expression is a female attractant. These results identify molecular mechanisms guiding domestication and adaptive responses to fluctuating sociality.social selection | sexy sons | epigenetics W ild animals bred in captivity have been observed to adapt to domestication within 10 generations (1-4). As a result, captive bred animals often have reduced fitness when reintroduced to natural conditions (5). Selective pressures disrupted by captivity include inbreeding avoidance, effective population size, disease exposure, predation, and sexual selection. For the latter example, evidence suggests that lack of social context for mate choice mediates adaptation to captivity (6). This context is especially relevant for social animals because the opportunity for mating success is regulated by hierarchical behavioral networks (i.e., social selection) (7), and this information is missing in captivity. The molecular mechanisms underlying phenotypes affected by lack of social selection are poorly understood. Furthermore, rapid adaptation to captivity raises questions about the roles of genetic inheritance vs. transgenerational effects (i.e., inheritance independent of genetic variation) (8). Resolving the mechanistic and hereditary basis of these transitions can provide insight into the flexibilit...

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Rapid Evolution of Egg Size in Captive Salmon

Cited by 261 publications

References 27 publications

Genetic adaptation to captivity can occur in a single generation

Genetic adaptation to captivity can occur in a single generation

Indirect genetic effects underlie oxygen-limited thermal tolerance within a coastal population of chinook salmon

Reintroducing domesticated wild mice to sociality induces adaptive transgenerational effects on MUP expression

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