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Targeted conservation genetics of the endangered chimpanzee

Heredity volume 125, pages15–27(2020)Cite this article

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Abstract

Populations of the common chimpanzee (Pan troglodytes) are in an impending risk of going extinct in the wild as a consequence of damaging anthropogenic impact on their natural habitat and illegal pet and bushmeat trade. Conservation management programmes for the chimpanzee have been established outside their natural range (ex situ), and chimpanzees from these programmes could potentially be used to supplement future conservation initiatives in the wild (in situ). However, these programmes have often suffered from inadequate information about the geographical origin and subspecies ancestry of the founders. Here, we present a newly designed capture array with ~60,000 ancestry informative markers used to infer ancestry of individual chimpanzees in ex situ populations and determine geographical origin of confiscated sanctuary individuals. From a test panel of 167 chimpanzees with unknown origins or subspecies labels, we identify 90 suitable non-admixed individuals in the European Association of Zoos and Aquaria (EAZA) Ex situ Programme (EEP). Equally important, another 46 individuals have been identified with admixed subspecies ancestries, which therefore over time, should be naturally phased out of the breeding populations. With potential for future re-introduction to the wild, we determine the geographical origin of 31 individuals that were confiscated from the illegal trade and demonstrate the promises of using non-invasive sampling in future conservation action plans. Collectively, our genomic approach provides an exemplar for ex situ management of endangered species and offers an efficient tool in future in situ efforts to combat the illegal wildlife trade.

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Fig. 1: Subspecies ancestry and inbreeding in wild and captive populations of chimpanzees.
Fig. 2: Hybrid classification.
Fig. 3: Geographical origin estimates for sanctuary individuals.
Fig. 4: Ancestry and geographical origin estimates from non-invasive samples.

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Acknowledgements

The authors would like to thank all institutions who provided samples for this study: The EAZA Biobank, Stichting AAP Amersfoort Zoo, Antwerp Zoo, Zoo Delle Star ad Aprilia, Royal Burgers’ Zoo Arnhem, Monde Sauvage Safari, Badoca Safari Park, Barcelona Zoo, Zoo Parc de Beauval, Bioparc Valencia, Borås Zoo, Parco Natura Viva, Edinburgh Zoo, Ölands Zoo, Plättli Zoo, Givskud Zoo/Zootopia, Safaripark Beekse Bergen, Hodonin Zoo, Xanthus Zoo, Kolmården Zoo, Krakow Zoo, Kristiansand Zoo, Lagos Zoo, Le Pal Zoo, Leipzig Zoo, Liberec Zoo, Lisbon Zoo, Madrid Zoo, Magdeburg Zoo, Olmense Zoo, Zoo Osnabrück, African Safari, Plaisance du Touch, Plzen Zoo, Centro de Rescate de Primates Rainfer, Zoological Center Tel Aviv—Ramat Gan, Safari Ravenna, Zoo di Roma, Leintal Zoo, Serengeti-park Hodenhagen, Reserve Africaine de Sigean, Wilhelma Zoo, Loro Parque Zoo, Touroparc, Twycross Zoo, AAP Primadomus, Warsaw Zoo, Schwabenpark, Zagreb Zoo, Cente International de Recherches Médicales de Franceville, Chimfunshi Wildlife Orphanage, Jeunes Animaux Confisques au Katanga, Ngamaba Island Chimpanzee Sanctuary, Tacugama Chimpanzee Sanctuary, The Chimpanzee Conservation Center. We further wish to thank Tom de Jongh and Lisbeth Borbye for valuable language editing and comments to the manuscript and Abigail Ramsøe for early developmental stages of the hybrid classification model. PF is supported by the Innovation Fund Denmark doctoral fellowship programme and the Candys Foundation. CF is supported by “la Caixa” doctoral fellowship programme. TSK is funded by Carlsberg grant CF19-0712 prepared within the framework of the HSE University Basic Research Program. TMB is supported by BFU2017-86471-P (MINECO/FEDER, UE), U01 MH106874 grant, Howard Hughes International Early Career, Obra Social “La Caixa” and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC 2017 SGR 880). EL is supported by CGL2017-82654-P (MINECO/FEDER, UE).

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Author notes

  1. These authors contributed equally: Peter Frandsen, Claudia Fontsere

  2. These authors jointly supervised this work: Tomas Marques-Bonet, Christina Hvilsom

Affiliations

  1. Research and Conservation, Copenhagen Zoo, Roskildevej 38, 2000, Frederiksberg, Denmark

    Peter Frandsen, Frands Carlsen & Christina Hvilsom

  2. Section for Computational and RNA Biology, Department of Biology, University of Copenhagen, Ole Maaløes Vej 5, 2200, Copenhagen, Denmark

    Peter Frandsen, Kristian Hanghøj & Hans Redlef Siegismund

  3. Institute of Evolutionary Biology, (UPF-CSIC), PRBB, Dr. Aiguader 88, 08003, Barcelona, Spain

    Claudia Fontsere, Esther Lizano, Jessica Hernandez-Rodriguez & Tomas Marques-Bonet

  4. Bioinformatics Research Center, Department of Mathematics, Aarhus University, C. F. Møllers Allé 8, 8000, Aarhus C, Denmark

    Svend Vendelbo Nielsen, Natalia Castejon-Fernandez & Thomas Mailund

  5. Institut Català de Paleontologia Miquel Crusafant, Universitat Autònoma de Barcelona, Edifici ICTA-ICP, c/ Columnes s/n, Cerdanyala del Vallès, 08193, Barcelona, Spain

    Esther Lizano & Tomas Marques-Bonet

  6. MRC Integrative Epidemiology Unit at University of Bristol, Bristol, BS8 2BN, UK

    David Hughes

  7. Population Health Sciences, Bristol Medical School, University of Bristol, Bristol, BS8 2BN, UK

    David Hughes

  8. GLOBE, Section for Geogenetics, Øster Voldgade 5-7, 1350, Copenhagen, Denmark

    Thorfinn Sand Korneliussen

  9. National Research University, Higher School of Economics, 20 Myasnitskaya Ulitsa, 101000, Moscow, Russia

    Thorfinn Sand Korneliussen

  10. Catalan Institution of Research and Advanced Studies (ICREA), Passeig de Lluís Companys 23, 08010, Barcelona, Spain

    Tomas Marques-Bonet

  11. CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri I Reixac, 408028, Barcelona, Spain

    Tomas Marques-Bonet

Authors
  1. Peter Frandsen
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  2. Claudia Fontsere
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  6. Esther Lizano
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  13. Tomas Marques-Bonet
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  14. Christina Hvilsom
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Corresponding authors

Correspondence to Peter Frandsen or Claudia Fontsere.

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Frandsen, P., Fontsere, C., Nielsen, S.V. et al. Targeted conservation genetics of the endangered chimpanzee. Heredity 125, 15–27 (2020). https://doi.org/10.1038/s41437-020-0313-0

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