Life history variation is maintained by fitness trade-offs and negative frequency-dependent selection.

The maintenance of diverse life history strategies within and among species remains a fundamental question in ecology and evolutionary biology. By using a near-complete 16-year pedigree of 12,579 winter-run steelhead (Oncorhynchus mykiss) from the Hood River, Oregon, we examined the continued maintenance of two life history traits: the number of lifetime spawning events (semelparous vs. iteroparous) and age at first spawning (2-5 years). We found that repeat-spawning fish had more than 2.5 times the lifetime reproductive success of single-spawning fish. However, first-time repeat-spawning fish had significantly lower reproductive success than single-spawning fish of the same age, suggesting that repeat-spawning fish forego early reproduction to devote additional energy to continued survival. For single-spawning fish, we also found evidence for a fitness trade-off for age at spawning: older, larger males had higher reproductive success than younger, smaller males. For females, in contrast, we found that 3-year-old fish had the highest mean lifetime reproductive success despite the observation that 4- and 5-year-old fish were both longer and heavier. This phenomenon was explained by negative frequency-dependent selection: as 4- and 5-year-old fish decreased in frequency on the spawning grounds, their lifetime reproductive success became greater than that of the 3-year-old fish. Using a combination of mathematical and individual-based models parameterized with our empirical estimates, we demonstrate that both fitness trade-offs and negative frequency-dependent selection observed in the empirical data can theoretically maintain the diverse life history strategies found in this population.

Genetic adaptation to captivity can occur in a single generation.

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.

How much does inbreeding contribute to the reduced fitness of hatchery-born steelhead (Oncorhynchus mykiss) in the wild?

Many declining populations are supplemented with captive-born individuals that are released directly into the wild. Because captive-born individuals can have lower fitness in the wild than their wild-born counterparts, a comprehensive understanding of the mechanisms responsible for the reduced fitness of these individuals is required for appropriate conservation and management decisions. Inbreeding among captive-born individuals is one plausible mechanism because captive breeding programs frequently use small numbers of breeders to create large numbers of siblings that are subsequently released together into the wild. We tested this hypothesis in a supplementation program for steelhead (Oncorhynchus mykiss) from the Hood River, Oregon, for which first-generation hatchery fish were demonstrated to have lower fitness in the wild than their wild-born counterparts. To determine the contribution of inbreeding to this fitness decline, we first assigned 11 run-years of hatchery steelhead (3005 fish) back to their broodstock parents (462 fish) using 8 polymorphic microsatellite loci. By combining pedigree analyses with species-specific estimates of genetic load, we found that inbreeding could at most account for a 1-4% reduction in the fitness of hatchery fish relative to wild fish. Thus, inbreeding alone cannot adequately explain the 15% average fitness decline observed in first-generation hatchery fish from this population.

A single generation of domestication heritably alters the expression of hundreds of genes.

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.