Chimpanzee genomic diversity reveals ancient admixture with bonobos

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Science  28 Oct 2016:
Vol. 354, Issue 6311, pp. 477-481
DOI: 10.1126/science.aag2602
  • Fig. 1 Chimpanzee geography and genetic substructure.

    (A) Geographic distribution of Pan populations. Reported coordinates for chimpanzee individuals are shown as circles colored by broad region of origin. Grouping is based on prior information about geographical origin (table S1), with lines connecting to clustered locations within the current range of subspecies. No further coordinates were available for Equatorial Guinea and Nigeria-Cameroon. DRC, Democratic Republic of the Congo. (B and C) PCA plots of chromosome 21 single-nucleotide polymorphism data for (B) central and (C) eastern chimpanzees. PCA coordinates were modified by Procrustes transformation. Samples of unknown origin are colored in gray. Circles, high-coverage genomes; squares, low-coverage genomes; triangles, chromosome 21 captured from fecal samples. These GPS-labeled samples cluster within the range of regional genetic variation reported in whole-genome sampling.

  • Fig. 2 Genome-wide statistics support gene flow between chimpanzees and bonobos.

    (A) Population-wise D statistic of the form D(X,Y; bonobos, human). Error bars correspond to two standard errors. Nonwestern chimpanzees share more derived alleles with bonobos than western chimpanzees do. (B) Western and central chimpanzee allele sharing with bonobos, binned by derived allele frequency in bonobos (Dj); bonobo alleles are more often shared with central chimpanzees across bonobo allele frequencies. Top, real data; middle, simulations without gene flow; bottom, simulations of a model with gene flow into nonwestern chimpanzees. Lines of best fit are in gray. (C) Western and central chimpanzee allele sharing with bonobos, stratified by both bonobo and chimpanzee derived allele frequency, calculated at a given frequency in bonobos and at least one of the chimpanzee subspecies (the color gradient represents the extent of sharing). (D) Divergence between chimpanzee subspecies versus minimum divergence to bonobos at sites with bonobo derived allele frequencies of ≥90% in windows of 50 kbp. Error bars represent 95% confidence intervals from 500 bootstrap replicates. Segments in the genomes of central chimpanzees with low divergence to bonobos show high divergence to western chimpanzees. Top, real data; middle, simulated data without gene flow; bottom, simulated data with gene flow.

  • Fig. 3 Conceptual model of a complex population history.

    SFS-based modeling indicates several contacts between chimpanzees and bonobos after their divergence. Split times (thousands of years ago, kya) and migration rates correspond to 95% confidence intervals obtained with the demographic model with western, central, and eastern chimpanzees (10). Gene flow is quantified as the scaled migration rate (2Nm). Red arrows, gene flow from bonobos into chimpanzees. The ancestral population of central and eastern chimpanzees received the highest amount of bonobo alleles, whereas central chimpanzees received additional, more recent gene flow (<200,000 years ago). Blue arrows, highest inferred migrations within chimpanzee subspecies (intense gene flow between central and eastern chimpanzees). α (dotted line), putative ancient gene flow between the ancestors of all chimpanzees and bonobos. β, more recent gene flow from chimpanzees into bonobos. Shaded area, range of estimates across all chimpanzee populations. γ, admixture between Nigeria-Cameroon and central and eastern chimpanzees; indirect gene flow from bonobos into Nigeria-Cameroon chimpanzees might have occurred through these contacts. δ, divergence time between western and Nigeria-Cameroon chimpanzees, estimated by using MSMC2 (10).

  • Fig. 4 Introgressed segments and inferred age of introgressed haplotypes.

    (A) Numbers of putatively introgressed heterozygous segments per population (top of each bar) and percentage of the chimpanzee genome that they constitute (bars). Dark bars represent segments uniquely found in each population; gray bars represent simulated data without gene flow. (B) Age distribution of bonobo-like haplotypes in chimpanzee populations, as estimated by ARGweaver. Chimpanzee subspecies are compared pairwise, and bonobo-like haplotypes are defined as regions of at least 50 kbp that coalesce within the bonobo subtree before coalescing with the other chimpanzee population (inset). Error bars represent 95% confidence intervals across Markov chain Monte Carlo replicates (10).

Supplementary Materials

  • Chimpanzee genomic diversity reveals ancient admixture with bonobos

    Marc de Manuel, Martin Kuhlwilm, Peter Frandsen, Vitor C. Sousa, Tariq Desai, Javier Prado-Martinez, Jessica Hernandez-Rodriguez, Isabelle Dupanloup, Oscar Lao, Pille Hallast, Joshua M. Schmidt, José María Heredia-Genestar, Andrea Benazzo, Guido Barbujani, Benjamin M. Peter, Lukas F. K. Kuderna, Ferran Casals, Samuel Angedakin, Mimi Arandjelovic, Christophe Boesch, Hjalmar Kühl, Linda Vigilant, Kevin Langergraber, John Novembre, Marta Gut, Ivo Gut, Arcadi Navarro, Frands Carlsen, Aida M. Andrés, Hans. R. Siegismund, Aylwyn Scally, Laurent Excoffier, Chris Tyler-Smith, Sergi Castellano, Yali Xue, Christina Hvilsom, Tomas Marques-Bonet

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Materials and Methods
    • Figs. S1 to S58
    • Tables S1 to S19
    • References
    Data S1

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