Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Genetic evidence for complex speciation of humans and chimpanzees

Abstract

The genetic divergence time between two species varies substantially across the genome, conveying important information about the timing and process of speciation. Here we develop a framework for studying this variation and apply it to about 20 million base pairs of aligned sequence from humans, chimpanzees, gorillas and more distantly related primates. Human–chimpanzee genetic divergence varies from less than 84% to more than 147% of the average, a range of more than 4 million years. Our analysis also shows that human–chimpanzee speciation occurred less than 6.3 million years ago and probably more recently, conflicting with some interpretations of ancient fossils. Most strikingly, chromosome X shows an extremely young genetic divergence time, close to the genome minimum along nearly its entire length. These unexpected features would be explained if the human and chimpanzee lineages initially diverged, then later exchanged genes before separating permanently.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Genetic relationships differ from species relationships.
Figure 2: Near a region of HG, CG or HC clustering, τ(x ) deviates strikingly and significantly from the genome average.
Figure 3: Reduced human–chimpanzee time divergence across chromosome X.

Similar content being viewed by others

References

  1. Zuckerkandl, E. & Pauling, L. Molecules as documents of evolutionary history. J. Theor. Biol. 8, 357–366 (1965)

    Article  CAS  PubMed  Google Scholar 

  2. Glazko, G. V. & Nei, M. Estimation of divergence times for major lineages of primate species. Mol. Biol. Evol. 20, 424–434 (2003)

    Article  CAS  PubMed  Google Scholar 

  3. Pamilo, P. & Nei, M. Relationships between gene trees and species trees. Mol. Biol. Evol. 5, 568–583 (1988)

    CAS  PubMed  Google Scholar 

  4. Ruvolo, M. Molecular phylogeny of the hominoids: inferences from multiple independent DNA sequence data sets. Mol. Biol. Evol. 14, 248–265 (1997)

    Article  CAS  PubMed  Google Scholar 

  5. Chen, F. C. & Li, W. H. Genomic divergences between humans and other hominoids and the effective population size of the common ancestor of humans and chimpanzees. Am. J. Hum. Genet. 68, 444–456 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Takahata, N. & Satta, Y. Evolution of the primate lineage leading to modern humans: phylogenetic and demographic inferences from DNA sequences. Proc. Natl Acad. Sci. USA 94, 4811–4815 (1997)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  7. Wall, J. D. Estimating ancestral population sizes and divergence times. Genetics 163, 395–404 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Rannala, B. & Yang, Z. Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164, 1645–1656 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  9. O'hUigin, C., Satta, Y., Takahata, N. & Klein, J. Contribution of homoplasy and of ancestral polymorphism to the evolution of genes in anthropoid primates. Mol. Biol. Evol. 19, 1501–1513 (2002)

    Article  CAS  PubMed  Google Scholar 

  10. Pilbeam, D. & Young, N. Hominoid evolution: synthesizing disparate data. C. R. Palevol. 3, 305–321 (2004)

    Article  Google Scholar 

  11. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  12. Mikkelsen, T. S. et al. Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437, 69–87 (2005)

    Article  CAS  Google Scholar 

  13. Hwang, D. G. & Green, P. Bayesian Markov chain Monte Carlo sequence analysis reveals varying neutral substitution patterns in mammalian evolution. Proc. Natl Acad. Sci. USA 101, 13994–14001 (2004)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  14. Rat Genome Sequencing Project Consortium, Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature 428, 493–521 (2004)

    Article  Google Scholar 

  15. Taylor, J., Tyekucheva, S., Zody, M., Chiaromonte, F. & Makova, K. D. Strong and weak male mutation bias at different sites in the primate genomes: Insights from the human–chimpanzee comparison. Mol. Biol. Evol. 23, 565–573 (2006)

    Article  CAS  PubMed  Google Scholar 

  16. Makova, K. D. & Li, W. H. Strong male-driven evolution of DNA sequences in humans and apes. Nature 416, 624–626 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Brunet, M. et al. A new hominid from the Upper Miocene of Chad. Nature 418, 145–151 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Vignaud, P. et al. Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418, 152–155 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Brunet, M. et al. New material of the earliest hominid from the Upper Miocene of Chad. Nature 434, 752–755 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  20. MacLatchy, L., Gebo, D., Kityo, R. & Pilbeam, D. Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion. J. Hum. Evol. 38, 1–25 (2000)

    Article  Google Scholar 

  21. Senut, B. et al. First hominid from the Miocene (Lukeino Formation, Kenya). C. R. Acad. Sci. IIA 332, 137–144 (2001)

    Google Scholar 

  22. WoldeGabriel, G. et al. Geology and palaeontology of the Late Miocene Middle Awash valley, Afar rift, Ethiopia. Nature 412, 175–178 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Sarich, V. M. in New Interpretations of Ape and Human Ancestry (eds Ciochon, R. L. & Corruccini, R. S.) 137–150 (Plenum, New York, 1983)

    Google Scholar 

  24. Coyne, J. A. & Orr, H. A. in Speciation and its Consequences (eds Otte, D. & Endler, J. A.) 180–207 (Sinauer, Sunderland, Massachusetts, 1989)

    Google Scholar 

  25. Tao, Y., Chen, S., Hartl, D. L. & Laurie, C. C. Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. Genetics 164, 1383–1397 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

  26. True, J. R., Weir, B. S. & Laurie, C. C. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics 142, 819–837 (1996)

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Orr, H. A. & Irving, S. Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics 169, 671–682 (2005)

    Article  PubMed  PubMed Central  Google Scholar 

  28. Haldane, J. B. S. Sex ratio and unidirectional sterility in hybrid animals. J. Genet. 58, 237–242 (1922)

    Article  Google Scholar 

  29. Tucker, P. K., Sage, R. D., Wilson, A. C. & Eichler, E. M. Abrupt cline for sex chromosomes in a hybrid zone between two species of mice. Evolution Int. J. Org. Evolution 46, 1146–1163 (1992)

    Article  Google Scholar 

  30. Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, New York, 1942)

    Google Scholar 

  31. Coyne, J. A. & Orr, H. A. Speciation (Sinauer, Sunderland, Massachusetts, 2004)

    Google Scholar 

  32. Rieseberg, L. H. Hybrid origin of plant species. Annu. Rev. Ecol. Syst. 28, 359–389 (1997)

    Article  Google Scholar 

  33. Boag, P. T. & Grant, P. R. The classical case of character release: Darwin's finches (Geospiza) on Isla Daphne Major, Galápagos. Biol. J. Linn. Soc. 22, 243–287 (1984)

    Article  Google Scholar 

  34. Schwarz, D., Matta, B. M., Shakir-Botteri, N. L. & McPheron, B. A. Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436, 546–549 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  35. Barton, N. H. The role of hybridization in evolution. Mol. Ecol. 10, 551–568 (2001)

    Article  CAS  PubMed  Google Scholar 

  36. Osada, N. & Wu, C. I. Inferring the mode of speciation from genomic data: a study of the great apes. Genetics 169, 259–264 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Jaffe, D. B. et al. Whole-genome sequence assembly for mammalian genomes: Arachne 2. Genome Res. 13, 91–96 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Schwartz, S. et al. Human–mouse alignments with BLASTZ. Genome Res. 13, 103–107 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Huang, X. On global sequence alignment. Comput. Appl. Biosci. 10, 227–235 (1994)

    CAS  PubMed  Google Scholar 

  40. Cheng, Z. et al. A genome-wide comparison of recent chimpanzee and human segmental duplications. Nature 437, 88–93 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  41. Blanchette, M. et al. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res. 14, 708–715 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Benson, G. Tandem repeats finder: a program to analyse DNA sequences. Nucleic Acids Res. 27, 573–580 (1999)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Steiper, M. E., Young, N. M. & Sukarna, T. Y. Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid-cercopithecoid divergence. Proc. Natl Acad. Sci. USA 101, 17021–17026 (2004)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank B. Bodamer, J. Caswell, M. Clamp, J. Coyne, J. Cuff, E. Green, G. McDonald, J. Mullikin, H. A. Orr, D. Page, D. Pilbeam, N. Stange-Thomann and M. Zody for discussions, comments and assistance with stages of this study, and E. Green, R. Gibbs and R. Wilson for producing and making publicly available data from large-scale sequencing projects (contiguous data from chromosomes 7 and X, and the orangutan and macaque shotgun data). N.P. was supported by a career transition award from the National Institutes of Health. E.S.L. was supported in part by funds from the National Human Genome Research Institute and the Broad Institute of Harvard and the Massachusetts Institute of Technology. D.R. was supported in part by a Burroughs–Wellcome Career Development Award in the Biomedical Sciences.Author Contributions The authors all played significant roles in the conception, execution, interpretation and presentation of the study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Reich.

Ethics declarations

Competing interests

To obtain sequencing reads from the NCBI trace archive (http://www.ncbi.nlm.nih.gov/Traces), use the following queries: (1) Gorilla data (Gorilla gorilla): CENTER_NAME = ‘WIBR’ and CENTER_PROJECT = ‘G611’ CENTER_NAME = ‘WIBR’ and CENTER_PROJECT = ‘G612’ CENTER_NAME = ‘WIBR’ and CENTER_PROJECT = ‘G618’ CENTER_NAME = ‘WIBR’ and CENTER_PROJECT = ‘G619’ CENTER_NAME = ‘WIBR’ and CENTER_PROJECT = ‘G744’; (2) New world monkey data (Ateles geoffroyi): CENTER_NAME = ‘WIBR’ and CENTER_PROJECT = ‘G820’. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Methods, Supplementary Tables 1–12, Supplementary Figure 1 and Supplementary Notes. This file also contains additional references. (PDF 971 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Patterson, N., Richter, D., Gnerre, S. et al. Genetic evidence for complex speciation of humans and chimpanzees. Nature 441, 1103–1108 (2006). https://doi.org/10.1038/nature04789

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04789

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing