The bonobo genome compared with the chimpanzee and human genomes

Journal name:
Nature
Volume:
486,
Pages:
527–531
Date published:
DOI:
doi:10.1038/nature11128
Received
Accepted
Published online

Two African apes are the closest living relatives of humans: the chimpanzee (Pan troglodytes) and the bonobo (Pan paniscus). Although they are similar in many respects, bonobos and chimpanzees differ strikingly in key social and sexual behaviours1, 2, 3, 4, and for some of these traits they show more similarity with humans than with each other. Here we report the sequencing and assembly of the bonobo genome to study its evolutionary relationship with the chimpanzee and human genomes. We find that more than three per cent of the human genome is more closely related to either the bonobo or the chimpanzee genome than these are to each other. These regions allow various aspects of the ancestry of the two ape species to be reconstructed. In addition, many of the regions that overlap genes may eventually help us understand the genetic basis of phenotypes that humans share with one of the two apes to the exclusion of the other.

At a glance

Figures

  1. Geographical distribution and test for admixture between chimpanzees and bonobos.
    Figure 1: Geographical distribution and test for admixture between chimpanzees and bonobos.

    a, Geographical distribution of bonobos and chimpanzees. b, D statistics for the admixture test between bonobos and three chimpanzee groups. Each pairwise comparison between one bonobo and two chimpanzee groups is depicted as one panel. Each point in a panel represents one bonobo individual compared with two chimpanzee individuals from different groups. Admixture between bonobo and chimpanzee is indicated by a Z-score greater than 4.4 or less than −4.4.

  2. Segmental duplications and transposon accumulation.
    Figure 2: Segmental duplications and transposon accumulation.

    a, Venn diagram showing segmental duplications in the human (H), chimpanzee (C) and bonobo (B) genomes. Each number of megabases refers to the total amount of sequence that occurs in segmental duplications (Supplementary Information, section 4). b, Accumulation of different retrotransposon classes on each lineage.

  3. Incomplete lineage sorting.
    Figure 3: Incomplete lineage sorting.

    a, Schematic description of ILS states and percentage of bases assigned to each state. b, Effective population sizes and split times inferred from ILS and based on a molecular clock with a mutation rate of 10−9yr−1. Myr, million years. We note that other estimates of mutation rates will correspondingly affect the estimates of the split times. c, Overlap between predicted ILS transposons and the closest HMM ILS assignments within 100bp of a transposon insertion. d, Proportion of ILS in exons, introns and across the whole genome, counted within ~1-Mb segments of alignment (Supplementary Information, section 8). e, Proportion of ILS dependent on recombination rates. Errors, 95% confidence interval.

  4. X/A ratios.
    Figure 4: X/A ratios.

    The X/A ratios for Ulindi (bonobo), an African human and a European human were inferred from heterozygosity, and that for the Pan ancestor was inferred from ILS. The low X/A ratio for the European has been suggested to be due to demographic effects connected to migrating out of Africa30. Errors, 95% confidence interval (Supplementary Information, sections 8 and 9).

  5. Selection in the bonobo-chimpanzee common ancestor and chimpanzees.
    Figure 5: Selection in the bonobo–chimpanzee common ancestor and chimpanzees.

    a, Diversity in chimpanzee and bonobo around the region on chromosome 3 devoid of ILS. b, Regions where bonobos fall outside the variation of chimpanzee upstream of the MHC. The MHC region is not plotted because the SNP density is sparse there as a result of duplications. Five regions among the 50 longest regions are shown in yellow. Red points show posterior probabilities >0.8.

Accession codes

Primary accessions

Sequence Read Archive

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Author information

Affiliations

  1. Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany

    • Kay Prüfer,
    • Michael Siebauer,
    • Jeffrey M. Good,
    • Anne Fischer,
    • Susan E. Ptak,
    • Michael Lachmann,
    • Aida M. Andrés,
    • Janet Kelso &
    • Svante Pääbo
  2. Bioinformatics Research Centre, Aarhus University, DK-8000 Aarhus C, Denmark

    • Kasper Munch,
    • Asger Hobolth,
    • Julien Dutheil,
    • Thomas Mailund &
    • Mikkel H. Schierup
  3. Max F. Perutz Laboratories, University Vienna, A-1030 Vienna, Austria

    • Ines Hellmann
  4. Human Cancer Genetics Program and Department of Molecular Virology, Immunology and Medical Genetics, The Ohio State University Comprehensive Cancer Center, Columbus, Ohio 43210, USA

    • Keiko Akagi &
    • David E. Symer
  5. J. Craig Venter Institute, Rockville, Maryland 20850, USA

    • Jason R. Miller,
    • Brian Walenz &
    • Granger Sutton
  6. University of Maryland, College Park, Maryland 20742, USA

    • Sergey Koren
  7. 454 Life Sciences, Branford, Connecticut 06405, USA

    • Chinnappa Kodira,
    • Roger Winer &
    • James R. Knight
  8. Genome Technology Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA

    • James C. Mullikin
  9. MRC Functional Genomics Unit, Department of Physiology, Anatomy and Genetics, University of Oxford, South Parks Road, Oxford OX1 3QX, UK

    • Stephen J. Meader &
    • Chris P. Ponting
  10. The Wellcome Trust Centre for Human Genetics, Roosevelt Drive, Oxford OX3 7BN, UK

    • Gerton Lunter
  11. Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Kanagawa 226-8503, Japan

    • Saneyuki Higashino
  12. Department of Genome Sciences, University of Washington and the Howard Hughes Medical Institute, Seattle, Washington 98195, USA

    • Emre Karakoç,
    • Can Alkan,
    • Saba Sajjadian,
    • Mario Ventura,
    • Tomas Marques-Bonet &
    • Evan E. Eichler
  13. Sezione di Genetica-Dipartimento di Anatomia Patologica e Genetica, University of Bari, I-70125 Bari, Italy

    • Claudia Rita Catacchio &
    • Mario Ventura
  14. ICREA, Institut de Biologia Evolutiva (UPF-CSIC), 08003 Barcelona, Catalonia, Spain

    • Tomas Marques-Bonet
  15. Lola Ya Bonobo Bonobo Sanctuary, “Petites Chutes de la Lukaya”, Kinshasa, Democratic Republic of Congo

    • Claudine André
  16. Réserve Naturelle Sanctuaire à Chimpanzés de Tchimpounga, Jane Goodall Institute, Pointe-Noire, Republic of Congo

    • Rebeca Atencia
  17. Chimpanzee Sanctuary and Wildlife Conservation Trust (CSWCT), Entebbe, Uganda

    • Lawrence Mugisha
  18. Zoo Leipzig, D-04105 Leipzig, Germany

    • Jörg Junhold
  19. Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA

    • Nick Patterson
  20. Division of Biological Sciences, University of Montana, Missoula, Montana 59812, USA

    • Jeffrey M. Good
  21. International Center for Insect Physiology and Ecology, 00100 Nairobi, Kenya

    • Anne Fischer
  22. Department of Bioscience, Aarhus University, DK-8000 Aarhus C, Denmark

    • Mikkel H. Schierup
  23. Present address: Department of Computer Engineering, Bilkent University, Ankara 06800, Turkey.

    • Can Alkan

Contributions

K.P., K.M., I.H., K.A., J.R.M., B.W., S.K., G.S., C.K., R.W., J.R.K., J.C.M., S.J.M, C.P.P., G.L., S.H., A.H., J.D., E.K., C. Alkan, S.S., C.R.C., M.V., T.M.-B., E.E.E., N.P., M.S., J.M.G., A.F., S.E.P., M.L., D.E.S., T.M., M.H.S., A.M.A., J.K. and S.P. analysed genetic data. C. André, R.A., L.M. and J.J. provided samples. K.P., J.K. and S.P. wrote the manuscript.

Competing financial interests

C.K., R.W. and J.R.K. are employees of Roche/454 Life sciences, which developed the technology used for the sequencing of the genome studied here.

Corresponding authors

Correspondence to:

The bonobo genome assembly has been deposited with the International Nucleotide Sequence Database Collaboration (DDBJ/EMBL/GenBank) under the EMBL accession number AJFE01000000. 454 shotgun data of Ulindi have been made available through the NCBI Sequence Read Archive under study ID ERP000601; Illumina sequences of 19 chimpanzee and bonobo individuals are available under study ID ERP000602.

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Supplementary information

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  1. Supplementary Information (11.7M)

    This file contains Supplementary Text and Data sections 1-12, which include Supplementary Figures, Supplementary Tables and Supplementary References (see Contents for details).

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