Genetic adaptation to novel environments can occur on ecological timescales

Background/Question/Methods

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 (Oncorhynchus mykiss) released into the Hood River, Oregon.  Specifically, 12,700 fish, comprising 15 run-years, were genotyped at 8 polymorphic microsatellite loci.  Broodstock for the hatchery consisted of both wild-born and first-generation hatchery fish, and their offspring were released into the wild as smolts. 

Results/Conclusions

First-generation hatchery fish had nearly double the lifetime reproductive success (measured as the number of returning adult offspring) when spawned in captivity than 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.  To identify the specific traits selected upon in the hatchery, we used next generation sequencing of messenger RNA (RNA-seq) to identify sets of genes that are differentially expressed between first generation hatchery and wild fish reared in a common environment.  These results illustrate that profound evolutionary processes (i.e., genetic adaptation to different environments) can occur on ecological timescales.