Benefits and pitfalls of captive conservation genetic management: Evaluating diversity in scimitar-horned oryx to support reintroduction planning
Introduction
The management of wildlife populations for species conservation is changing. Traditional distinctions between captive and wild populations are giving way to a range of management scenarios that may be viewed as distributed along a continuum, from intensive control of individual animals throughout their lifetime, to extensive stewardship of populations across generations. Depending on the needs of the species and the pressures they face, different management scenarios may be found in unrestricted natural habitats, and in the wide variety of captive and semi-captive programmes (e.g. fenced protected areas) employed throughout the conservation community. For many endangered species, the global population is composed of multiple sub-populations managed in very different ways, either by accident or design. Metapopulation management, which integrates population management at a strategic level across multiple locations, is seen as beneficial to the long-term conservation of individual species. International and regional studbooks that support management of zoo populations across multiple regions, and strategic planning approaches such as the IUCN-SSC Conservation Planning Specialist Group’s One-Plan (Byers et al., 2013), explicitly set out to integrate captive breeding programmes with the management of natural populations, and represent examples of such coordination (Redford et al., 2012). The greater the importance of intensive management to a species, the greater the drive to achieve integration across its global populations; programmes seeking to reintroduce species that are extinct in the wild are therefore obvious candidates to benefit most from such an approach.
The reintroduction of any species is a complex process requiring a multi-disciplinary and usually multi-partner approach. A significant body of knowledge now exists on the factors impacting reintroduction success that has resulted in the production of comprehensive guidance and policy on the subject (IUCN/SSC, 2013). Nevertheless, every reintroduction is unique and the relative importance of the various biological, environmental and political criteria required to establish a sustainable wild population vary from species to species. Furthermore, bringing these conditions together in the same place at the same time can take many years. The scimitar-horned oryx (SHO), Oryx dammah, was formally distributed across north Africa, throughout countries bordering the Sahara desert, but was gradually lost through hunting and land-use competition, before finally disappearing from the Sahelo-Sahel region of Chad in the early 1980′s (Fig. 1) (Durant et al., 2014). As one of the most prominent and easily recognizable large mammals in the Sahelo-Saharan landscape, it represents a flagship species and its reintroduction should therefore benefit the ecology and conservation of the ecosystem as a whole. A project to reintroduce the SHO to Chad has been under development since around 2010, led by the Environment Agency – Abu Dhabi (EAD), the Chadian Ministere de l’Environnement et de la Peche, and the Sahara Conservation Fund, with the first animals arriving in Chad in 2016 (Soorae, 2018). Project activities include the application of a broad range of social and natural sciences, with a significant emphasis placed on ensuring that the most appropriate animals are available for establishing a new founder population.
Founder selection requires consideration of multiple biological factors, including taxonomy, evolutionary history, population genetic diversity, local adaptation, individual animal health and disease risk. Reintroduction guidelines emphasize the importance of genetic considerations in project planning to ensure that sufficient genetic diversity is present within the founders to minimize risks of inbreeding and to enable adaptation to future environmental change (IUCN/SSC, 2013). In widely distributed species it is also important to consider local genetic adaptation as a criterion in selecting the most appropriate candidate source populations. A substantial body of literature has been built-up on these issues over the past three decades, initially describing theoretical approaches to the genetic management of captive populations (Lacy, 1987; Ballou and Lacy, 1995; Ivy and Lacy, 2012) and founder selection (Tracy et al., 2011) before addressing the potential of molecular genetic analysis as a tools to directly inform captive management (Henkel et al., 2012; Fienieg and Galbusera, 2013; Ivy et al., 2016; Sato et al., 2017) and reintroduction decisions (e.g. the Eurasian beaver (Senn et al., 2014a); northern bald ibis (Wirtz et al., 2018); Tasmanian devils (Grueber et al., 2019)). While such examples are on the increase, it is still uncommon to undertake species-wide molecular genetic evaluations of candidate founders, using multiple DNA marker types to directly support conservation planning. Some previous work on SHO genetic diversity has been conducted (Iyengar et al., 2007), but relatively little is known about the level and distribution of genetic variation across the principle potential source populations. Within the development of the Chad SHO reintroduction programme, it was therefore decided that a more comprehensive characterisation of genetic diversity was required in order to meet best practice guidelines. In this paper we present a large-scale study of global molecular genetic diversity undertaken over ten years to support decisions about global transfer of scimitar-horned oryx and inform the reintroduction of SHOs to Chad.
According to available records, the captive population of SHOs was initially founded from 48 individuals taken from the wild in the 1960′s and used to start breeding programmes in the world’s zoos. Between 1963 and 1967, individuals were captured in Chad and divided between the USA (c.29), Europe (ca.17) and Japan (n = 2) (Woodfine and Gilbert, 2016). Some records exist of earlier collections from the 1930s (ca. 12), but these are not thought to have contributed to today’s international zoo populations. It is also likely that during the 1960s and 1970s further animals were obtained from the wild and held in private collections in countries on the Arabian Peninsula, such as the United Arab Emirates (UAE). Although no written documents to support this supposition appear to exist, the number of SHOs now present in the UAE strongly suggest this occurred. SHOs have bred well in captivity and over the past 40 years, the number of animals has increased to approximately 15,000 worldwide, primarily distributed in government and private holdings in the UAE and private owners in the USA, but also within the conservation breeding management programmes of Europe (European Association of Zoos and Aquariums – Endangered Species Programmes (EAZA-EEP)), the USA (Association of Zoos and Aquariums – Species Survival Plan (AZA-SSP)) and Australia (Zoo and Aquarium Association – Australasian Species Management Program (ZAA-ASMP)). While studbook records from the managed zoo programmes do exist, they are incomplete, with pedigrees containing a high percentage of unknown or uncertain relationships (Gilbert, 2018). A previous translocation of SHO to Tunisia using zoo animals from the EAZA-EEP and the AZA-SSP between 1985 and 2007 (Fig. 1) resulted in a number of semi-wild herds distributed across five protected areas which also now act as a reservoir of SHO genetic diversity (Gilbert et al. unpublished). More recently, the SHO has become one of the focal species within the Conservation Centers for Species Survival (C2S2) programme (Wildt et al., 2012) that is seeking to move towards extensive herd management of threatened antelope species in the USA. Given this population management history and associated lack of detailed pedigree information, it has been necessary to employ molecular genetic analysis to be able to address many of the genetic criteria within the reintroduction planning process.
An initial population genetic study by Iyengar et al. (2007), employed mitochondrial DNA (mtDNA) control region sequencing and nuclear DNA microsatellite genotyping at six loci to investigate captive diversity, primarily in the US and Europe. While no significant structuring was found in the microsatellite data, where overall diversity was found to be quite low, the mtDNA sequence data revealed as many as 40 ancestral maternal lineages, divided into three clades thought to have evolved separately around 2 million YBP. To inform founder selection in the ongoing reintroduction project, it was necessary to significantly expand this earlier work to increase the geographic scope and number of reference samples used to assess candidate founder populations, before conducting a more in-depth comparative population genetic analysis using genome-wide SNP DNA markers.
The potential of genomic approaches to enhance population genetic studies in terms of delivering greater resolution, estimating historic demographic change and investigating local adaptation is well-established (Allendorf et al., 2010), and there are now multiple examples where modern sequencing approaches have delivered significant new biological insights in wildlife species of conservation concern (Garner et al., 2016). However, the transfer of genomics into practical application in conservation management has been gradual (Shafer et al., 2015), due in part to the resources required for projects of this scale, together with technical considerations such as the need for plentiful high molecular weight DNA. Here we employed ddRAD sequencing, a method for screening thousands of nuclear SNP DNA markers across hundreds of samples, to provide an increased level of resolution between SHO populations and individuals, and thus enable better assessment of genetic diversity ahead of founder selection for reintroduction.
In addition to direct genetic assessment of SHO herds, the study provided the opportunity to evaluate an important issue associated with the use of molecular markers to measure genetic diversity in captivity. The extent to which genetic drift drives apparent population differentiation has been investigated in some natural systems (Weeks et al., 2016), but the implications for conservation breeding programmes have received little attention. When interpreting the results of observed population structure in conservation genetic studies it is necessary to determine the likelihood that such findings indicate pre-captive population differentiation that may be associated with adaptive divergence, or that the observed structure is an artefact of much more recent captive differentiation due to the effects of genetic drift in small isolated groups of animals. To this end, we investigated the effects of drift in captive SHOs on resulting population genetic structure, through a series of simulations.
We aimed to address the following principle management questions in relation to global genetic diversity and the reintroduction of the scimitar-horned oryx to Chad:
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How is genetic diversity distributed across geographic regions, oryx collections and among individuals throughout the world?
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How can measures of captive population genetic diversity be interpreted in relation to the roles of genetic drift or adaptive differentiation?
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At an individual level, is there any evidence of marked variation in measures of genetic diversity within source populations?
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How can these results be used to optimize the selection of founders for the Chad reintroduction programme?
Section snippets
Samples
Samples in this study were collected from six separate captive SHO populations, between the 2006 and 2014 (Table 1). Three populations are located within the United Arab Emirates at the following institutions: the Environment Agency of Abu Dhabi (EAD), Al Ain Zoo (AAZ) and the Dubai Desert Conservation Reserve (DDCR). The EAD population consists of several thousand oryx and is primarily composed of animals belonging to the late Sheikh Zayed bin Sultan Al Nahyan’s collection originally situated
Global scimitar-horned oryx diversity
Results of mitochondrial DNA sequencing revealed a total of 43 different control region haplotypes, inlcuding six novel sequences (Genbank Acc. MN689133-8). These formed a number of self-similar clusters separated by multiple DNA nucleotide substitutions (Fig. 2). The largest separation in the haplotype network corresponded to a broad division between samples from Arabia and the USA in one half and samples from Europe and Australia in the other half, although this pattern was by no means
Discussion
The results presented here comprise multiple genetic studies performed over the past ten years with the common aim of evaluating captive genetic diversity in scimitar-horned oryx to inform their reintroduction to the wild. Their combined strength lies in bridging the gap between intensively managed zoo populations with individual pedigree data, and extensively managed animal herds, which may comprise very large numbers of rare or endangered species, but for which almost nothing is known about
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Declaration of Competing Interest
The authors declare that they have no competing interest in relation to this manuscript.
Acknowledgements
The authors are grateful to two anonymous reviewers who helped to significantly improve earlier drafts of the manuscript. The authors would like to thank the following researchers who have contributed to the production of the three datasets: Ricardo Pusey, Louis Lignereux, Maria Elena Pesci, Carlos Rojo Solis, Ross McEwing, Liz Heap, Mary-Frances Roberts, Leonie Grenfell, Jennifer Kaden & staff at Edinburgh Genomics. Marie Petretto, Gian Lorenzo D’Alterio, Chawki Najjar, Hela Guedara and the Al
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These authors contributed equally to this work.