Chimpanzee genomic diversity reveals ancient admixture with bonobos

Abstract

Our closest living relatives, chimpanzees and bonobos, have a complex demographic history. We analyzed the high-coverage whole genomes of 75 wild-born chimpanzees and bonobos from 10 countries in Africa. We found that chimpanzee population substructure makes genetic information a good predictor of geographic origin at country and regional scales. Multiple lines of evidence suggest that gene flow occurred from bonobos into the ancestors of central and eastern chimpanzees between 200,000 and 550,000 years ago, probably with subsequent spread into Nigeria-Cameroon chimpanzees. Together with another, possibly more recent contact (after 200,000 years ago), bonobos contributed less than 1% to the central chimpanzee genomes. Admixture thus appears to have been widespread during hominid evolution.

Figure 1. Chimpanzee geography and genetic substructure

(A) Geographic distribution of Pan populations. Reported coordinates for individuals are shown as circles colored by broad region of origin. Grouping is based on prior information on geographical origin (Table S1), connected by lines to clustered locations within the current range of subspecies. No further coordinates were available for Equatorial Guinea and Nigeria-Cameroon. (B & C) PCA plot of chromosome 21 SNP data for central (B) and eastern (C) chimpanzees. PCA coordinates modified by Procrustes transformation. Samples with unknown origin colored in gray. Squares: Low coverage genomes. Triangles: Chromosome 21 captured from fecal samples. These GPS labelled samples cluster within the range of regional genetic variation reported in whole-genome sampling.

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

(A). Population-wise D-statistic of the form D(X, Y; Bonobos, Human). Non-western chimpanzees share more derived alleles with bonobos than western chimpanzees. (B) Western and central chimpanzee allele sharing with bonobos binned by derived allele frequency in bonobos (D_j); bonobo alleles are more often shared with central chimpanzees across bonobo frequencies. Real data (top panel); simulations without gene flow (middle); simulations of a model with gene flow into non-western chimpanzees (bottom). (C) Western and central chimpanzee allele sharing with bonobos stratified by both bonobo and chimpanzee derived allele frequency (D_jx), calculated at a given frequency in bonobos and at least one of the chimpanzee subspecies (color gradient representing the extent of sharing). (D) Divergence between chimpanzee subspecies versus minimum divergence to bonobos at sites with bonobo derived allele frequency ≥90% in windows of 50 Kbp. Error bars represent 95% confidence intervals from 500 bootstrap replicates. Segments with low divergence to bonobos in the genomes of central chimpanzees show high divergence to western chimpanzees. Real data (top), simulated data without gene flow (middle) and with gene flow (bottom).

Figure 3. Conceptual model of a complex population history

SFS-based modeling infers several contacts between chimpanzees and bonobos after their divergence. Split times (Kya) and migration rates correspond to 95% confidence intervals (CI) obtained with the demographic model with western, central and eastern chimpanzees (10). Quantification of gene flow as migration rates scaled by the effective size (2Nm). Red arrows: gene flow from bonobos into chimpanzees. The ancestral population of central and eastern chimpanzees received the highest amount of bonobo alleles, while central chimpanzees received additional, more recent gene flow (<200 Kya). 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 is inferred by the model. (β) More recent gene flow from chimpanzees into bonobos is inferred. Shaded area: Range of estimates across all chimpanzee populations. (γ) Inferred admixture between Nigeria-Cameroon and central/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 is estimated by using MSMC2 (10).

Figure 4. Introgressed segments and inferred age of introgressed haplotypes

(A) Numbers of putatively introgressed segments in heterozygosity per population, and proportion of the chimpanzee genome. Dark bars represent segments uniquely found in each population, grey bars simulations 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 across MCMC replicates (10).