Chimpanzee Genomic Diversity Reveals Ancient Admixture with Bonobos

Overview

Journal Science

Specialty Science

Date 2016 Oct 30

PMID 27789843

Citations 113

Authors

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

Jose Maria Heredia-Genestar

Andrea Benazzo

Guido Barbujani

Benjamin M Peter

Lukas F K Kuderna

Ferran Casals

Samuel Angedakin

Mimi Arandjelovic

Christophe Boesch

Hjalmar Kuhl

Linda Vigilant

Kevin Langergraber

John Novembre

Marta Gut

Ivo Gut

Arcadi Navarro

Frands Carlsen

Aida M Andres

Hans R Siegismund

Aylwyn Scally

Laurent Excoffier

Chris Tyler-Smith

Sergi Castellano

Yali Xue

Christina Hvilsom

Tomas Marques-Bonet

Affiliations

Soon will be listed here.

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.

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References

Frichot E, Mathieu F, Trouillon T, Bouchard G, Francois O . Fast and efficient estimation of individual ancestry coefficients. Genetics. 2014; 196(4):973-83. PMC: 3982712. DOI: 10.1534/genetics.113.160572. View

Li H, Durbin R . Inference of human population history from individual whole-genome sequences. Nature. 2011; 475(7357):493-6. PMC: 3154645. DOI: 10.1038/nature10231. View

Prufer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S . The complete genome sequence of a Neanderthal from the Altai Mountains. Nature. 2013; 505(7481):43-9. PMC: 4031459. DOI: 10.1038/nature12886. View

Slatkin M . Linkage disequilibrium--understanding the evolutionary past and mapping the medical future. Nat Rev Genet. 2008; 9(6):477-85. PMC: 5124487. DOI: 10.1038/nrg2361. View

Prado-Martinez J, Sudmant P, Kidd J, Li H, Kelley J, Lorente-Galdos B . Great ape genetic diversity and population history. Nature. 2013; 499(7459):471-5. PMC: 3822165. DOI: 10.1038/nature12228. View

Rasmussen M, Hubisz M, Gronau I, Siepel A . Genome-wide inference of ancestral recombination graphs. PLoS Genet. 2014; 10(5):e1004342. PMC: 4022496. DOI: 10.1371/journal.pgen.1004342. View

Burgess R, Yang Z . Estimation of hominoid ancestral population sizes under bayesian coalescent models incorporating mutation rate variation and sequencing errors. Mol Biol Evol. 2008; 25(9):1979-94. DOI: 10.1093/molbev/msn148. View

Meyer M, Kircher M . Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc. 2010; 2010(6):pdb.prot5448. DOI: 10.1101/pdb.prot5448. View

Green R, Krause J, Briggs A, Maricic T, Stenzel U, Kircher M . A draft sequence of the Neandertal genome. Science. 2010; 328(5979):710-722. PMC: 5100745. DOI: 10.1126/science.1188021. View

10.

Helgason A, Einarsson A, Gudmundsdottir V, Sigurdsson A, Gunnarsdottir E, Jagadeesan A . The Y-chromosome point mutation rate in humans. Nat Genet. 2015; 47(5):453-7. DOI: 10.1038/ng.3171. View

11.

Delaneau O, Marchini J, Zagury J . A linear complexity phasing method for thousands of genomes. Nat Methods. 2011; 9(2):179-81. DOI: 10.1038/nmeth.1785. View

12.

Gonder M, Locatelli S, Ghobrial L, Mitchell M, Kujawski J, Lankester F . Evidence from Cameroon reveals differences in the genetic structure and histories of chimpanzee populations. Proc Natl Acad Sci U S A. 2011; 108(12):4766-71. PMC: 3064329. DOI: 10.1073/pnas.1015422108. View

13.

McVicker G, Gordon D, Davis C, Green P . Widespread genomic signatures of natural selection in hominid evolution. PLoS Genet. 2009; 5(5):e1000471. PMC: 2669884. DOI: 10.1371/journal.pgen.1000471. View

14.

Henn B, Gignoux C, Jobin M, Granka J, Macpherson J, Kidd J . Hunter-gatherer genomic diversity suggests a southern African origin for modern humans. Proc Natl Acad Sci U S A. 2011; 108(13):5154-62. PMC: 3069156. DOI: 10.1073/pnas.1017511108. View

15.

Vernot B, Tucci S, Kelso J, Schraiber J, Wolf A, Gittelman R . Excavating Neandertal and Denisovan DNA from the genomes of Melanesian individuals. Science. 2016; 352(6282):235-9. PMC: 6743480. DOI: 10.1126/science.aad9416. View

16.

Hughes J, Skaletsky H, Pyntikova T, Graves T, van Daalen S, Minx P . Chimpanzee and human Y chromosomes are remarkably divergent in structure and gene content. Nature. 2010; 463(7280):536-9. PMC: 3653425. DOI: 10.1038/nature08700. View

17.

Funfstuck T, Arandjelovic M, Morgan D, Sanz C, Reed P, Olson S . The sampling scheme matters: Pan troglodytes troglodytes and P. t. schweinfurthii are characterized by clinal genetic variation rather than a strong subspecies break. Am J Phys Anthropol. 2014; 156(2):181-91. PMC: 4692250. DOI: 10.1002/ajpa.22638. View

18.

Won Y, Hey J . Divergence population genetics of chimpanzees. Mol Biol Evol. 2004; 22(2):297-307. DOI: 10.1093/molbev/msi017. View

19.

Nielsen R . Estimation of population parameters and recombination rates from single nucleotide polymorphisms. Genetics. 2000; 154(2):931-42. PMC: 1460954. DOI: 10.1093/genetics/154.2.931. View

20.

Becquet C, Przeworski M . A new approach to estimate parameters of speciation models with application to apes. Genome Res. 2007; 17(10):1505-19. PMC: 1987350. DOI: 10.1101/gr.6409707. View