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Conservation Genetics

, Volume 16, Issue 5, pp 1115–1126 | Cite as

Genetic structure of captive and free-ranging okapi (Okapia johnstoni) with implications for management

  • David W. G. StantonEmail author
  • Philippe Helsen
  • Jill Shephard
  • Kristin Leus
  • Linda Penfold
  • John Hart
  • Noëlle F. Kümpel
  • John G. Ewen
  • Jinliang Wang
  • Peter Galbusera
  • Michael W. Bruford
Research Article

Abstract

Breeding programs for endangered species increasingly use molecular genetics to inform their management strategies. Molecular approaches can be useful for investigating relatedness, resolving pedigree uncertainties, and for estimating genetic diversity in captive and wild populations. Genetic data can also be used to evaluate the representation of wild population genomes within captive population gene-pools. Maintaining a captive population that is genetically representative of its wild counterpart offers a means of conserving the original evolutionary potential of a species. Okapi, an even-toed ungulate, endemic to the Democratic Republic of Congo, have recently been reclassified as Endangered by the IUCN. We carried out a genetic assessment of the ex-situ okapi (Okapia johnstoni) population, alongside an investigation into the genetic structure of wild populations across their geographic range. We found that while levels of nuclear (12 microsatellite loci) genetic variation in the wild, founder and captive okapi populations were similar, mitochondrial (833 bp of Cyt b, CR, tRNA-Thr and tRNA-Pro) variation within captive okapi was considerably reduced compared to the wild, with 16 % lower haplotype diversity. Further, both nuclear and mitochondrial alleles present in captivity provided only partial representation of those present in the wild. Thirty mitochondrial haplotypes found in the wild were not found in captivity, and two haplotypes found in captivity were not found in the wild, and the patterns of genetic variation at microsatellite loci in our captive samples were considerably different to those of the wild samples. Our study highlights the importance of genetic characterisation of captive populations, even for well-managed ex-situ breeding programs with detailed studbooks. We recommend that the captive US population should be further genetically characterised to guide management of translocations between European and US captive populations.

Keywords

Captive Wild Ex-situ In-situ Founder 

Notes

Acknowledgments

We gratefully acknowledge the assistance of the Institut Congolais pour la Conservation de la Nature (ICCN) for allowing the field collection and export of samples. We would like to particularly thank the Wildlife Conservation Society (WCS), Gilman International Conservation (GIC) and the Okapi Conservation Project for their considerable assistance with the fieldwork in this study, and the amazing okapi conservation work that they carry out in the DRC. We also thank all the museum curators that sent historic samples or allowed us to collect them. In particular, from the Chicago Field Museum: Bill Stanley and Lawrence Heaney (with the help of Keith Dobney, Aberdeen Univ. and Greger Larson, Durham Univ); from Copenhagen NHM: Hans J. Baagøe, Kristian Gregersen and Mogens Andersen; from Paris NHM: Joséphine Lesur-Gebremariam; from the Royal Museum for Central Africa, Tervuren, Belgium: Wim Wendelen (with the help of Floris van der Sman). We thank the Frankfurt Zoological Society, the Wildlife Conservation Society, the Lukuru Foundation/TL2 project, the Zoological Society of London (ZSL), Marwell Zoo and the considerable number of people who assisted in various ways with sample collection. In particular, we would like to thank John Fataki Bolingo, Bryna Griffin, Terese Hart, Chrysostome Kaghoma, Luaison, John Lukas, Kambale Magloire, Ephrem Mpaka, Stuart Nixon, Elise Queslin, Alex Quinn, Rosemary Ruf and Ashley Vosper. This project was jointly funded by the UK Natural Environment Research Council (NERC) and ZSL (ZSL as NERC CASE industry partner and via an Erasmus Darwin Barlow Expedition grant). We also acknowledge the financial support provided by GIC (the Okapi Conservation Project), the US Fish and Wildlife Service, the UK’s Darwin Initiative and the Mohamed bin Zayed Species Conservation Fund. Finally, the CRC gratefully acknowledges the structural support of the Flemish Government.

Supplementary material

10592_2015_726_MOESM1_ESM.docx (69 kb)
Supplementary material 1 (DOCX 69 kb)
10592_2015_726_MOESM2_ESM.png (273 kb)
Fig. S1 Set one, hypotheses one and two for the AMOVA analysis. AMOVA groups are shown in grey boxes, and AMOVA populations are shown with a dashed outline. The AMOVA statistics for the hypothesis with the best explanatory power (highest significant among group variation) are shown in bold and outlined in red. Supplementary material 2 (PNG 272 kb)
10592_2015_726_MOESM3_ESM.png (331 kb)
Fig. S2 Set two, hypotheses three to six for the AMOVA analysis. AMOVA groups are shown in grey boxes, and AMOVA populations are shown with a dashed outline. The hypothesis with the best explanatory power (highest significant among group variation) are shown in bold and outlined in red. Supplementary material 3 (PNG 330 kb)
10592_2015_726_MOESM4_ESM.png (368 kb)
Fig. S3 Set three, hypotheses seven and eight for the AMOVA analysis. AMOVA groups are shown in grey boxes, and AMOVA populations are shown with a dashed outline. The hypothesis with the best explanatory power (highest significant among group variation) are shown in bold and outlined in red. Supplementary material 4 (PNG 367 kb)
10592_2015_726_MOESM5_ESM.png (237 kb)
Fig. S4 Set four, hypotheses nine to 13 for the AMOVA analysis. AMOVA groups are shown in grey boxes, and AMOVA populations are shown with a dashed outline. The hypothesis with the best explanatory power (highest significant among group variation) are shown in bold and outlined in red. Supplementary material 5 (PNG 236 kb)
10592_2015_726_MOESM6_ESM.png (284 kb)
Fig. S5 Boxplot of observed heterozygosity of founder, captive and wild okapi samples using microsatellite markers. Notches show 95 % confidence intervals. Supplementary material 6 (PNG 284 kb)
10592_2015_726_MOESM7_ESM.png (239 kb)
Fig. S6 Plot to identify the most likely number of genetic clusters, using the program STRUCTURE v2.3.4 (Pritchard et al. 2000) and the method of Evanno et al. (2005). The highest value of delta K indicates the most likely number of clusters. This was carried out for all samples used for the microsatellite analysis (“Founder/captive/wild”), and for the wild samples only (“Wild only”). Supplementary material 7 (PNG 239 kb)
10592_2015_726_MOESM8_ESM.png (35 kb)
Fig. S7 STRUCTURE plot of founder, captive and wild okapi samples for K = 4, using only F0 founders for the founder sample set. Numbers correspond to: 5) Captive (United States; n = 4), 6) Captive (Epulu, DRC; n = 8), 7) Captive Europe (n = 18), 8) Founders (F0 only; n = 12), 5) Wild (sampling region 1 [Fig. 1]; n = 17), 6) Wild (sampling region 2; n = 54), 7) Wild (sampling region 3; n = 3) and 8) Wild (sampling region 4; n = 6). Supplementary material 8 (PNG 34 kb)
10592_2015_726_MOESM9_ESM.png (47 kb)
Fig. S8 STRUCTURE plot of founder, captive and wild okapi samples, excluding related individuals (r > 0.25), for K = 4. Numbers correspond to: 5) Captive (United States; n = 4), 6) Captive (Epulu, DRC; n = 6), 7) Captive Europe (n = 9), 8) Founders (n = 12), 1) Wild (sampling region 1 [Fig. 1]; n = 13), 2) Wild (sampling region 2; n = 22), 3) Wild (sampling region 3; n = 3) and 4) Wild (sampling region 4; n = 6). Supplementary material 9 (PNG 47 kb)
10592_2015_726_MOESM10_ESM.png (465 kb)
Fig. S9 GENELAND plot of founder, captive and wild okapi samples for K = 4. Numbers correspond to: 5) Captive (United States; n = 4), 6) Captive (Epulu, DRC; n = 8), 7) Captive Europe (n = 18), 8) Founders (n = 16), 1) Wild (sampling region 1 [Fig. 1]; n = 17), 2) Wild (sampling region 2; n = 54), 3) Wild (sampling region 3; n = 3) and 4) Wild (sampling region 4; n = 6). Supplementary material 10 (PNG 464 kb)
10592_2015_726_MOESM11_ESM.png (422 kb)
Fig. S10 STRUCTURE plot of founder and captive samples only, using sampling information (the four sampling regions), and updating allele frequencies using only the wild samples to attempt to assign the founder individuals to a part of the wild okapi distribution. Numbers correspond to: 1) Founders (F0 and F1; n = 16), 2) Wild (sampling region 1 [Fig. 1]; n = 17), 3) Wild (sampling region 2; n = 54), 4) Wild (sampling region 3; n = 3) and 5) Wild (sampling region 4; n = 6). Supplementary material 11 (PNG 421 kb)
10592_2015_726_MOESM12_ESM.png (356 kb)
Fig. S11 STRUCTURE plot of wild samples only for K = 3. Numbers correspond to: 1) Wild (sampling region 1; Fig. 1; N = 17), 2) Wild (sampling region 2; N = 54), 3) Wild (sampling region 3; N = 3) and 4) Wild (sampling region 4; N = 6). Supplementary material 12 (PNG 356 kb)
10592_2015_726_MOESM13_ESM.docx (10 kb)
Supplementary material 13 (DOCX 10 kb)
10592_2015_726_MOESM14_ESM.xlsx (61 kb)
Supplementary material 14 (XLSX 60 kb)

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Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • David W. G. Stanton
    • 1
    Email author
  • Philippe Helsen
    • 2
    • 9
  • Jill Shephard
    • 2
    • 3
  • Kristin Leus
    • 4
  • Linda Penfold
    • 5
  • John Hart
    • 6
  • Noëlle F. Kümpel
    • 7
  • John G. Ewen
    • 8
  • Jinliang Wang
    • 8
  • Peter Galbusera
    • 2
  • Michael W. Bruford
    • 1
  1. 1.School of BiosciencesCardiff UniversityCardiffUK
  2. 2.Centre for Research and ConservationRoyal Zoological Society of AntwerpAntwerpBelgium
  3. 3.School of Veterinary and Life SciencesMurdoch UniversityPerthAustralia
  4. 4.Conservation Breeding Specialist Group, European Regional NetworkCopenhagen ZooMerksemBelgium
  5. 5.South-East Zoo Alliance for Reproduction and Conservation (SEZARC)YuleeUSA
  6. 6.Lukuru FoundationProjet Tshuapa-Lomami-Lualaba (TL2)KinshasaDemocratic Republic of the Congo
  7. 7.Conservation ProgrammesZoological Society of LondonLondonUK
  8. 8.Institute of ZoologyZoological Society of LondonLondonUK
  9. 9.Evolutionary Ecology GroupUniversity of AntwerpAntwerpBelgium

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