Logistical constraints often mean that captive populations are dispersed among multiple zoos, aquaria and wildlife parks. Many institutions will each house only a handful of individuals from a particular species, and this could have serious repercussions for long-term genetic diversity. Successful captive breeding therefore often requires cooperation between institutions to create what is effectively human-mediated gene flow between very small populations. This has been facilitated by a number of enterprises, including the Species Survival Program (SSP) of the American Zoo and Aquarium Association, which was started in 1981 as a cooperative conservation programme for selected species in zoos and aquaria in North America. This programme currently oversees the captive breeding of 161 different species, most of which involve many different institutes. The SSP for the golden lion tamarin, for example, is based on a captive population that is currently comprised of 445 individuals distributed around 150 different zoos.
This type of cooperation is needed if captive breeding programmes are to achieve a commonly stated goal of maintaining 90 % of genetic diversity for a period of 100 years while increasing the inbreeding levels by no more than 10 %. The effective population size needed to maintain genetic diversity for this length of time will depend to some extent on the generation time of the species in question. Assuming that the population size remains constant, and note that we are talking about Ne and not Nc, the necessary effective population size has been derived from the the rate at which heterozygosity is expected to decline within populations of different sizes following genetic drift (Frankham, Ballou and Briscoe 2002; see also Chapter 3), and is approximately equal to:
where L is the generation length in years. The inverse relationship between generation length and the Ne necessary for the maintenance of genetic diversity is shown in Figure 7.12. The tremendous range in generation times between species means that the minimum desirable Ne of captively bred populations will vary enormously; in some insects a generation will last only a few days, whereas in Caribbean flamingoes (Phoenicopterus ruber) it may last 26 years.
Maintaining 90 % of genetic diversity while avoiding inbreeding may be an unrealistic goal in many captively bred species, although good management can minimize the loss of diversity. We know from earlier chapters that the Ne of populations, captive or otherwise, will be influenced by a number of factors, and all of these must be taken into account if maximum genetic diversity is to be maintained. A bottleneck, for example, will have a lasting effect on a population's Ne, and although careful management can often maintain populations at stable numbers, bottlenecks caused by founder effects are not uncommon during the establishment of captive populations. The IUCN recommends that a captive
g 2000 z
1 2 3 4 5 6 Generation length (years)
Figure 7.12 Relationship between generation length and the minimum Ne that is necessary if genetic diversity is to be maintained in captive populations. The necessary Ne rapidly increases as generation times become smaller population be established before the number of wild individuals drops below 1000, so that an adequate number (20--30) of unrelated individuals can be used as founders. Unfortunately, such forward planning is not always possible and captive populations are founded all too often by only a handful of individuals (recall the earlier example of Pere David's deer). Variation in reproductive success (VRS) will also influence the Ne of a captive population. Some species, including those with a socially monogamous mating system (e.g. many birds), can often be managed so as to increase the proportion of breeding adults. In other species (e.g. many mammals) breeding is most successful under a polygamous mating system, in which case the VRS of males may be high (Chapter 6).
Associated with the maintenance of genetic diversity is inbreeding avoidance. This is harder to achieve in small captive populations, although careful management using pedigree information and estimates of relatedness (Chapter 6) can minimize the amount of inbreeding depression that a population may suffer. Molecular data may be particularly useful for this because pedigree information on the founders of captive populations may never be complete. Almost no pedigree information was available for the captive population of the St Vincent parrot (Amazona guildingii), which currently comprises around 72 individuals. This is a protected species, but the 1987 Wildlife Protection Act allowed people who had birds of their own to give them up without being prosecuted. As a result, these birds came from multiple, often anonymous, sources so there was essentially no information on their relatedness or their wild population of origin. Microsatellite data were used to estimate the relatedness between all pairs of individuals, and this formed the basis for a breeding programme that would maximize genetic diversity and minimize inbreeding (Russello and Amato, 2004).
Whenever population sizes permit, every effort should be made to avoid matings between relatives, particularly as inbreeding depression that is not evident in captive populations may manifest itself once individuals are released into the wild. Captive inbred males of the African butterfly Bicyclus anynana showed a small decrease in mating success when in their cages, but when they were later released into a large tropical greenhouse it became apparent that the inbred males were substantially less fit than other males (Joron and Brakefield, 2003). Cases such as this mean that, when in doubt, inbreeding should be avoided as much as possible even if inbreeding depression is not evident in captivity. When population sizes are small, the inbreeding coefficient will increase rapidly from one generation to the next (Equation 7.1; Figure 7.5). Because many zoos have only a few representatives of each species, individuals are often moved around between institutions for the purposes of breeding. However, the benefits of this in terms of reduced inbreeding must be balanced against the stress to the individuals, the potential transmission of diseases, and the reduction in Ne that can follow the loss of population subdivisions.
Overall, captive breeding is costly, challenging and does not provide a long-term solution for the conservation of species. Although it may be considered the last resort for preserving a species, we shall see in the final section that there are actually even more desperate attempts under way to preserve genetic diversity for the future.
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