ABSTRACT:
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. In many cases, fish hatcheries, for example, such population structures 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 programs 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 terminated. 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 transformation that can eventually lead to natural population no longer capable of sustaining themselves.
QUOTES FROM THE TEXT:
Managers of endangered populations face a double-jeopardy situation. On the one hand, failure to intervene when it is clear that a species is declining derministically can lead to a scenario where extinction is virtually certain. On the other hand, the use of captive propagation for supplementation purposes can result in genetic changes that may reduce the ability of a wild population to be self-sustaining. Captive environments can be radically different from natural habitats, and there is little question that their inhabitants can often rapidly undergo significant evolutionary change for morphological, behavioral, and physiological traits in ways that compromise fitness in a more natural setting. This has become particularly apparent in the case of hatchery populations of salmonids.
When members of a captive population are introduced into the wild, the introgression of conditionally deleterious mutations (either neutral or promoted by selection in captivity) can impose a genetic load on the wild population. Our purpose is to investigate whether this load can develop sufficiently rapidly and to a high enough magnitude to significantly magnify the risk of extinction of natural populations on time scales of relevance to conservation biologists.
The results clearly show that captive propagation programs that impose relaxed (or positive) selection on alleles that are otherwise deleterious in nature can have a pronounced negative effect on the genetic fitness of the natural population, the magnitude of which depends on the pattern of gene flow and the sizes of the two populations.
In the context of a population subject to external supplementation, the loss of adaptation to the natural habitat is expected to be most severe when genes spend substantial fractions of time in the captive environment and migrants from the captive population make a large contribution to the pool of breeding individuals in the wild each generation. Such conditions imply that the captive population segment is the dominate contributor to the entire productivity of the species, a condition that results in the accumulation of alleles that are neutral (or beneficial) in captivity but deleterious in nature. As such a scenario progresses, a supplementation program that is initially intended as a temporary productivity boost can eventually transform the wild population to a state such that complete collapse would occur in the absence of continued supplementation. In other words, the short-term demographic advantages of supplementation programs not only promote genetic changes that are contrary to long-term population persistence, but in doing so, they can lead to the highly undesirable situation in which continued persistence of individuals in the wild is possible without permanent reliance on the supplementation program. Such a condition presents a particularly difficult management problem. On the one hand, the wild population has become entirely reliant on the captive population for subsidization. On the other hand, prolongation of the captive breeding program is likely to only exacerbate the situation by promoting the eventual fixation of more deleterious mutations.
·alleles that are deleterious in nature but favored in captivity can become fixed in large as well as small populations, and may even be more common in the former, as larger populations are more likely to harbor rare conditionally advantageous alleles.
In principle, a wild population can readapt to the natural environment after it has been released from a supplementation program, assuming that fixation of deleterious alleles have not caused permanent damage. However, if the prior supplementation load is so high that the population is unable to replace itself on a per-generation basis, recovery would require that the rate of re-adaptation offset the consequences of demographic decline. This may be difficult in many situations, as the return to wild-type fitness can require several dozens of generation, especially if the wild population had previously experienced substantial gene flow from the captive population.
It is clear that long-term supplementation programs whose primary goal is to provide a demographic boost to a natural population are particularly incompatible with the preservation of the fitness of the original wild population.
In summary, the consequences of gene flow from domesticated populations raise serious concerns about the use of supportive breeding programs to enhance the ability of a natural population to sustain harvesting, or to enhance genetic diversity.
·long-term supplementation programs appear to be incompatible with the permanent maintenance of self-sustaining wild populations, unless the two population segments are kept in a state of long-term reproductive isolation.