Abstract
Conservation breeding programs such as zoos play a major role in preventing extinction, but their sustainability may be impeded by neutral and adaptive population genetic change. These changes are difficult to detect for a single species or context, and impact global conservation efforts. We analyse pedigree data from 15 vertebrate species – over 30,000 individuals – to examine offspring survival over generations of captive breeding. Even accounting for inbreeding, we find that the impacts of increasing generations in captivity are highly variable across species, with some showing substantial increases or decreases in offspring survival over generations. We find further differences between dam and sire effects in first- versus multi-generational analysis. Crucially, our multispecies analysis reveals that responses to captivity could not be predicted from species’ evolutionary (phylogenetic) relationships. Even under best-practice captive management, generational fitness changes that cannot be explained by known processes (such as inbreeding depression), are occurring.
Highlights
Conservation breeding programs such as zoos play a major role in preventing extinction, but their sustainability may be impeded by neutral and adaptive population genetic change
Genetic changes as a result of captive breeding have been demonstrated to occur in as little as a single generation in steelhead trout[11], so conservation breeding programs are unlikely to be immune to the effects of adaptation to captivity
We used multi-species mixed-effects models to investigate the effect of generations in captivity on offspring survival to reproductive maturity in 15 vertebrate species encompassing over 30,000 data points whilst accounting for inbreeding, parental age, year effects, regions and species phylogeny
Summary
Conservation breeding programs such as zoos play a major role in preventing extinction, but their sustainability may be impeded by neutral and adaptive population genetic change. A recent systematic review and meta-analysis investigating birth origin effects on reproductive success revealed captive-born animals have substantially lower reproductive success in captivity than their wild-born counterparts, for offspring survival traits[12]. This result seems to conflict with the expectation of improved fitness in captivity (e.g.13); many of the studies reviewed considered only the first generation (G1) of captive breeding. It is essential to disentangle first generation and multi-generational changes when investigating adaptation to captivity Other genetic factors such as inbreeding can contribute substantially to fitness changes over time in small populations
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