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.

  • Letter
  • Published:

Fine-scale recombination patterns differ between chimpanzees and humans

Nature Genetics volume 37, pages 429–434 (2005)Cite this article

A Corrigendum to this article was published on 01 April 2005

Abstract

Recombination rates seem to vary extensively along the human genome. Pedigree analysis suggests that rates vary by an order of magnitude when measured at the megabase scale1, and at a finer scale, sperm typing studies point to the existence of recombination hotspots2. These are short regions (1–2 kb) in which recombination rates are 10–1,000 times higher than the background rate. Less is known about how recombination rates change over time. Here we determined to what degree recombination rates are conserved among closely related species by estimating recombination rates from 14 Mb of linkage disequilibrium data in central chimpanzee and human populations. The results suggest that recombination hotspots are not conserved between the two species and that recombination rates in larger (50 kb) genomic regions are only weakly conserved. Therefore, the recombination landscape has changed markedly between the two species.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Comparison of hotspots in the two species.
Figure 2: Percentage of hotspots detected as shared under two models.
Figure 3: Concordance of total ρ for chimpanzee and human samples.
Figure 4: Correlation in total ρ if recombination rates are the same in the two species.

Similar content being viewed by others

References

  1. Kong, A. et al. A high-resolution recombination map of the human genome. Nat. Genet. 31, 241–247 (2002).

    Article  CAS  PubMed  Google Scholar 

  2. Kauppi, L., Jeffreys, A.J. & Keeney, S. Where the crossovers are: recombination distributions in mammals. Nat. Rev. Genet. 5, 413–424 (2004).

    Article  CAS  PubMed  Google Scholar 

  3. Stumpf, M.P. & McVean, G.A. Estimating recombination rates from population-genetic data. Nat. Rev. Genet. 4, 959–968 (2003).

    Article  CAS  PubMed  Google Scholar 

  4. Crawford, D.C. et al. Evidence for substantial fine-scale variation in recombination rates across the human genome. Nat. Genet. 36, 700–706 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Fearnhead, P. Consistency of estimators of the population–scaled recombination rate. Theor. Popul. Biol. 64, 67–79 (2003).

    Article  PubMed  Google Scholar 

  6. Li, N. & Stephens, M. Modeling linkage disequilibrium and identifying recombination hotspots using single-nucleotide polymorphism data. Genetics 165, 2213–2233 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. McVean, G.A. et al. The fine-scale structure of recombination rate variation in the human genome. Science 304, 581–584 (2004).

    Article  CAS  PubMed  Google Scholar 

  8. Cullen, M., Perfetto, S.P., Klitz, W., Nelson, G. & Carrington, M. High-resolution patterns of meiotic recombination across the human major histocompatibility complex. Am. J. Hum. Genet. 71, 759–776 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Kong, A. et al. Recombination rate and reproductive success in humans. Nat. Genet. 36, 1203–1206 (2004).

    Article  CAS  PubMed  Google Scholar 

  10. Wall, J.D., Frisse, L.A., Hudson, R.R. & Di Rienzo, A. Comparative linkage-disequilibrium analysis of the beta-globin hotspot in primates. Am. J. Hum. Genet. 73, 1330–1340 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ptak, S.E. et al. Absence of the TAP2 human recombination hotspot in chimpanzees. PLoS Biol. 2, 849–855 (2004).

    Article  CAS  Google Scholar 

  12. Hinds, D.A. et al. Whole genome patterns of common DNA variation in diverse human populations. Science (in the press).

  13. Britten, R.J. Divergence between samples of chimpanzee and human DNA sequences is 5%, counting indels. Proc. Natl. Acad. Sci. USA 99, 13633–13635 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ebersberger, I., Metzler, D., Schwarz, C. & Paabo, S. Genomewide comparison of DNA sequences between humans and chimpanzees. Am. J. Hum. Genet. 70, 1490–1497 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. de Massy, B. Distribution of meiotic recombination sites. Trends Genet. 19, 514–522 (2003).

    Article  CAS  PubMed  Google Scholar 

  16. Petes, T.D. Meiotic recombination hot spots and cold spots. Nat. Rev. Genet. 2, 360–369 (2001).

    Article  CAS  PubMed  Google Scholar 

  17. Haring, S.J., Halley, G.R., Jones, A.J. & Malone, R.E. Properties of natural double-strand-break sites at a recombination hotspot in Saccharomyces cerevisiae. Genetics 165, 101–114 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Shiroishi, T., Sagai, T., Hanzawa, N., Gotoh, H. & Moriwaki, K. Genetic control of sex–dependent meiotic recombination in the major histocompatibility complex of the mouse. EMBO J. 10, 681–686 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Jeffreys, A.J. & Neumann, R. Reciprocal crossover asymmetry and meiotic drive in a human recombination hot spot. Nat. Genet. 31, 267–271 (2002).

    Article  CAS  PubMed  Google Scholar 

  20. Jeffreys, A.J., Murray, J. & Neumann, R. High-resolution mapping of crossovers in human sperm defines a minisatellite-associated recombination hotspot. Mol. Cell 2, 267–273 (1998).

    Article  CAS  PubMed  Google Scholar 

  21. Patil, N. et al. Blocks of limited haplotype diversity revealed by high–resolution scanning of human chromosome 21. Science 294, 1719–1723 (2001).

    Article  CAS  PubMed  Google Scholar 

  22. Altshul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

    Article  Google Scholar 

  23. Stephens, M. & Donnelly, P. A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am. J. Hum. Genet. 73, 1162–1169 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Stephens, M., Smith, N.J. & Donnelly, P. A new statistical method for haplotype reconstruction from population data. Am. J. Hum. Genet. 68, 978–989 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Dutilleul, P. Modifying the t-test for assessing the correlation between two spatial processes. Biometrics 49, 305–314 (1993).

    Article  Google Scholar 

  26. Hudson, R.R. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18, 337–338 (2002).

    Article  CAS  PubMed  Google Scholar 

  27. Fischer, A., Wiebe, V., Paabo, S. & Przeworski, M. Evidence for a complex demographic history of chimpanzees. Mol. Biol. Evol. 21, 799–808 (2004).

    Article  CAS  PubMed  Google Scholar 

  28. Ptak, S.E., Voelpel, K. & Przeworski, M. Insights into recombination from patterns of linkage disequilibrium in humans. Genetics 167, 387–397 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank M. Lachmann, M. Stephens, K. Voepel and J. Wall for computer programs; M. Lachmann, M. Stephens and Rechenzentrum Garching (especially H. Lederer and W. Nagel) for computer support; D. Cox, M. Lachmann, S. Myers, J. Pritchard and M. Stephens for discussions; A. Di Rienzo for comments on the manuscript; N. Shen for her efforts in the hybrid analyses and resequencing array hybridizations; and M. Jen and K. Pant for their contributions to SNP discovery and base calling efforts. P. Morin helped oversee the collection and management of the chimpanzee samples. Support for this work was provided by the Max Planck Society and a Deutsche Forshungsgesellschaft grant to S.P.

Author information

Author notes

  1. Molly Przeworski, Kelly A Frazer and Svante Pääbo: These authors contributed equally to this work.

Authors and Affiliations

  1. Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6 04103, Leipzig, Germany

    Susan E Ptak, Kathrin Koehler, Birgit Nickel & Svante Pääbo

  2. Perlegen Sciences, Inc., 2021 Stierlin Court, Mountain View, 94043, California, USA

    David A Hinds, Nila Patil, Dennis G Ballinger & Kelly A Frazer

  3. Department of Ecology and Evolutionary Biology, Brown University, 80 Waterman Street, Box G-W, Providence, 02912, Rhode Island, USA

    Molly Przeworski

Authors
  1. Susan E Ptak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A Hinds
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kathrin Koehler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Birgit Nickel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nila Patil
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dennis G Ballinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Molly Przeworski
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kelly A Frazer
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Svante Pääbo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susan E Ptak.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Comparison of the method and data used here with results from two sperm typing experiments for the MHC region. (PDF 205 kb)

Supplementary Fig. 2

Allele frequency distribution for the chimpanzee and human data. (PDF 88 kb)

Supplementary Table 1

Observed frequency of hotspots. (PDF 66 kb)

Supplementary Table 2

Results from power simulations. (PDF 68 kb)

Supplementary Table 3

Simulation results for other demographic assumptions. (PDF 83 kb)

Supplementary Note (PDF 63 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ptak, S., Hinds, D., Koehler, K. et al. Fine-scale recombination patterns differ between chimpanzees and humans. Nat Genet 37, 429–434 (2005). https://doi.org/10.1038/ng1529

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng1529

This article is cited by

Search

Advanced 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