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Ancient admixture from an extinct ape lineage into bonobos

Nature Ecology & Evolution volume 3, pages 957–965 (2019)Cite this article

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An Author Correction to this article was published on 14 May 2019

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Abstract

Admixture is a recurrent phenomenon in humans and other great ape populations. Genetic information from extinct hominins allows us to study historical interactions with modern humans and discover adaptive functions of gene flow. Here, we investigate whole genomes from bonobo and chimpanzee populations for signatures of gene flow from unknown archaic populations, finding evidence for an ancient admixture event between bonobos and a divergent lineage. This result reveals a complex population history in our closest living relatives, probably several hundred thousand years ago. We reconstruct up to 4.8% of the genome of this ‘ghost’ ape, which represents genomic data of an extinct great ape population. Genes contained in archaic fragments might confer functional consequences for the immunity, behaviour and physiology of bonobos. Finally, comparing the landscapes of introgressed regions in humans and bonobos, we find that a recurrent depletion of introgression is rare, suggesting that genomic incompatibilities arose seldom in these lineages.

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Fig. 1: Trees of putatively introgressed fragments.
Fig. 2: Analysis of putatively introgressed windows.
Fig. 3: Model of population history in Pan species with archaic gene flow into bonobos.
Fig. 4: Posterior values of the models used.
Fig. 5: Distribution of introgression across the genome.

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Data availability

Sequence data from a previous study are publicly available under the accession code PRJEB15086 at the European Nucleotide Archive. Genotype data are available at http://biologiaevolutiva.org/tmarques/data/. Data pertaining to the results are in the Supplementary Information.

Change history

  • 14 May 2019

    In the version of this article originally published, a funding acknowledgement was missing for Tomas Maques-Bonet. The original funding statement was: “T.M.-B. was supported by MINECO BFU2014-55090-P (FEDER), a U01 MH106874 grant, the Howard Hughes International Early Career programme, Obra Social ‘La Caixa’ and Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement de la Generalitat de Catalunya.” It has been updated to: “T.M.-B. was supported by BFU2017-86471-P (MINECO/FEDER, UE), a U01 MH106874 grant, the Howard Hughes International Early Career programme, 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).” The error has been corrected in the HTML and PDF versions of this article.

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Acknowledgements

We thank A. M. Andres, B. Vernot and L. J. Kuhlwilm for comments and discussion, and M. de Manuel for help with the data. M.K. was supported by a DFG fellowship (KU 3467/1-1). V.C.S. was supported by the Fundação para a Ciência e a Tecnologia (project UID/BIA/00329/2013) and EU Horizon 2020 programme (Marie Skłodowska-Curie grant 799729). L.E. was supported by the Swiss National Science Foundation (number 310030B-166605). T.M.-B. was supported by BFU2017-86471-P (MINECO/FEDER, UE), a U01 MH106874 grant, the Howard Hughes International Early Career programme, 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).

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Authors and Affiliations

  1. Institut de Biologia Evolutiva, (CSIC-Universitat Pompeu Fabra), Parc de Recerca Biomèdica de Barcelona, Barcelona, Spain

    Martin Kuhlwilm, Sojung Han & Tomas Marques-Bonet

  2. Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal

    Vitor C. Sousa

  3. Institute of Ecology and Evolution, University of Berne, Berne, Switzerland

    Vitor C. Sousa & Laurent Excoffier

  4. Swiss Institute of Bioinformatics, Lausanne, Switzerland

    Laurent Excoffier

  5. National Centre for Genomic Analysis–Centre for Genomic Regulation, Barcelona Institute of Science and Technology, Barcelona, Spain

    Tomas Marques-Bonet

  6. Institucio Catalana de Recerca i Estudis Avançats, Barcelona, Spain

    Tomas Marques-Bonet

  7. Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain

    Tomas Marques-Bonet

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  1. Martin Kuhlwilm
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Contributions

M.K., S.H., V.C.S. and L.E. analysed the data. M.K. and T.M.-B. wrote the manuscript.

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Correspondence to Martin Kuhlwilm or Tomas Marques-Bonet.

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Supplementary information

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Supplementary methods and analysis, Supplementary Figures 1–32

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Supplementary Tables

Supplementary Tables 1–21

Supplementary Data

Principal component analysis (PCA) of putatively introgressed fragments.

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Kuhlwilm, M., Han, S., Sousa, V.C. et al. Ancient admixture from an extinct ape lineage into bonobos. Nat Ecol Evol 3, 957–965 (2019). https://doi.org/10.1038/s41559-019-0881-7

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