Captive breeding and the genetic fitness of natural populations

Many populations of endangered species are subject to recurrent introductions of individuals from an alternative setting where selection is either relaxed or in a direction opposite to that in the natural habitat. Such population structures, which are common to captive breeding and hatchery programs, can lead to a scenario in which alleles that are deleterious (and ordinarily kept at low levels) in the wild can rise to high frequencies and, in some cases, go to fixation. We outline how these genetic responses to supplementation can develop to a large enough extent to impose a substantial risk of extinction for natural populations on time scales of relevance to conservation biology. The genetic supplementation load can be especially severe when a captive population that is largely closed to import makes a large contribution to the breeding pool of individuals in the wild, as these conditions insure that the productivity of the two-population system is dominated by captive breeders. However, a substantial supplementation load can even develop when the captive breeders are always derived from the wild, and in general, a severe restriction of gene flow into the natural population is required to reduce this load to an insignificant level. Domestication selection (adaptation to the captive environment) poses a particularly serious problem because it promotes fixations of alleles that are deleterious in nature, thereby resulting in a permanent load that cannot be purged once the supplementation program is truncated. Thus, our results suggest that the apparent short-term demographic advantages of a supplementation program can be quite deceiving. Unless the selective pressures of the captive environment are closely managed to resemble those in the wild, long-term supplementation programs are expected to result in genetic transformations that can eventually lead to natural populations that are no longer capable of sustaining themselves.