On the horns of a dilemma: molecular approaches refine ex situ conservation in crisis

Authors


Michael A. Russelo, Fax: 250 807 8005; E-mail: michael.rusello@ubc.ca

Abstract

Seven years into this new millennium, species and habitat loss continue at an accelerated rate. While there have been individual examples of conservation success, the trend towards catastrophic loss of biological diversity persists. If we are to be successful in saving even a handful of critically endangered species, it is clear that they will need to be intensively managed using a variety of in situ and ex situ approaches. The highest profile ex situ conservation strategy is captive breeding. Although its relative role in an overall conservation management plan varies, captive breeding may present the only viable option for propagating the future of a species once rendered extinct in the wild. The study of Iyengar et al. in this issue of Molecular Ecology on one such species, the scimitar-horned oryx (Oryx dammah), represents an important contribution to ex situ conservation, demonstrating how critical insights into demographic history and population genetic structure obtained using molecular approaches may significantly contribute to captive breeding and reintroduction strategies.

Precisely how effective captive breeding is for conservation varies with the particular taxon, threats, and interconnectivity with other management strategies. The issue of how broadly useful this approach has been — or will be — has been controversial and, at times, acrimonious (Caughley 1994; Snyder et al. 1996). In many cases, it has appeared to be a ‘straw man’ argument related more to competing priorities and resources (e.g. diverting funds from in situ conservation) than to a critical examination of its past and potential utility. What does seem clear, however, is that ex situ population management will become increasingly important in the future. In the most extreme cases, where species are extinct in the wild and only persist in captivity, captive breeding may represent the only viable strategy for ameliorating their complete loss. In order to be effective as a conservation tool and overcome the serious challenges associated with maintaining small populations ex situ (e.g. inbreeding depression, selection for the captive environment), captive breeding programs must be scientifically managed, incorporating all available demographic and genetic information (Russello & Amato 2004).

Iyengar et al. (2007) provide the first genetic study of the scimitar-horned oryx (Oryx dammah), now considered extinct in the wild, but represented by a large number of individuals in captivity (Fig. 1). The authors reconstructed patterns of mitochondrial DNA (mtDNA) and nuclear microsatellite variation within and among captive management programmes administered by the Species Survival Plan (SSP) and the European Endangered Species Programme (EEP). In order to increase temporal and spatial sampling (the vast majority of captive founders were captured in Chad), the authors also utilized historical DNA analysis of museum specimens collected in Sudan (1911) and Chad (1925). Phylogenetic and network analyses of mtDNA control region sequence data revealed deep divergences among extant scimitar-horned oryx haplotypes, with estimated divergence times ranging from 2.1 million to 2.7 million years. The authors examined these reconstructed patterns in light of recent geological history of North Africa, concluding that the high mtDNA divergence recovered within this once widespread species was the result of the restriction of populations within Pleistocene glacial refugia followed by population expansion during interglacial periods. This reconstructed demographic history relative to palaeoclimatic events, combined with what is known of the life history of the scimitar-horned oryx (e.g. migratory, travelling large distances) have contributed to the high levels of genetic diversity maintained across populations. Although likely panmictic across its historical range, Iyengar et al. (2007) revealed that both mtDNA haplotypic and microsatellite genotypic variation were unevenly distributed across the captive populations managed by the SSP in North America relative to participating institutions within the EEP-managed programme and additional populations from South Africa (SA) and United Arab Emirates (UAB). These data identified genetically important individuals in the SSP, SA and UAB populations, and suggested the need for assisted gene flow across programmes to maximum representation of the remaining lineages of the scimitar-horned oryx.

Figure 1.

The scimitar-horned oryx (Oryx dammah) is thought to be extinct in the wild, but survives in captivity. Photo credit: Lisa M. Ware.

These results have important conservation implications for future management of the scimitar-horned oryx and highlight the complex issues associated with managing, maintaining, and if appropriate, reintroducing genetically and demographically healthy groups back into the wild. These challenges necessitate the development of new approaches and paradigms in order to maximize the effectiveness of ex situ population management as a conservation tool. Employing new technologies to obtain detailed genotypic data offer exciting improvements upon the traditional strategies of assuming that all founders are equally unrelated and valuable (Jones et al. 2002; Russello & Amato 2004). Such data also allow for identification of genetically important individuals and an empirical assessment of whether current management and husbandry techniques are meeting conservation goals. This is especially important in herd and colonial species that cannot be maintained in simple breeding pairings that form the basis of current zoo-based genetic management plans. For species with sufficient representation in natural history museum collections, historical DNA analysis provides another avenue for innovation, offering the potential for reconstructing the gene pool of recently diminished or extirpated populations. Knowledge of allele frequency distributions of in situ populations before decline allows for empirical assessments of the genetic consequences of population bottlenecks (Bouzat et al. 1998) and, more importantly for ex situ population management, enhances the ability to estimate the degree to which genetic variation formerly found in natural populations is represented within captivity. As a common goal of captive population management is to preserve the genetic variation of the wild population from which the founders were drawn (Lacy 1994), knowledge of the historical allele frequency distribution provides the baseline level to which management programmes may strive.

Anthropogenic changes are driving an unparalleled extinction crisis on the planet. New paradigms of intensive species management will be necessary to save an increasing number of endangered species. The application of emerging molecular and population genetic approaches within ex situ conservation programmes, including those employed in Iyengar et al. (2007) and discussed here, offers an opportunity for humans to slow this trend.

Michael Russello is an Assistant Professor at the University of British Columbia Okanagan with research interests in vertebrate conservation genetics, molecular ecology and population genomics. George Amato is the Director of the Sackler Institute for Comparative Genomics at the American Museum of Natural History. His research interests are primarily concerned with integrating novel genetic and genomic approaches with applied management programs for small, fragmented populations of endangered species.

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