Y chromosome sequence variation and the history of human populations (original) (raw)

Nature Genetics volume 26, pages 358–361 (2000)Cite this article

Abstract

Binary polymorphisms associated with the non-recombining region of the human Y chromosome (NRY) preserve the paternal genetic legacy of our species that has persisted to the present, permitting inference of human evolution, population affinity and demographic history1. We used denaturing high-performance liquid chromatography (DHPLC; ref. 2) to identify 160 of the 166 bi-allelic and 1 tri-allelic site that formed a parsimonious genealogy of 116 haplotypes, several of which display distinct population affinities based on the analysis of 1062 globally representative individuals. A minority of contemporary East Africans and Khoisan represent the descendants of the most ancestral patrilineages of anatomically modern humans that left Africa between 35,000 and 89,000 years ago.

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References

  1. Hammer, M.F. & Zegura, S.L. The role of the Y chromosome in human evolutionary studies. Evol. Anthropol. 5, 116–134 (1996).
    Article Google Scholar
  2. Oefner, P.J. & Underhill, P.A. DNA mutation detection using denaturing high-performance liquid chromatography. Current Protocols in Human Genetics. Suppl 19, 7.10.1– 7.10.12 (Wiley & Sons, New York, 1998).
    Google Scholar
  3. Underhill, P.A. et al. Detection of numerous Y chromosome biallelic polymorphisms by denaturing high performance liquid chromatography (DHPLC). Genome Res. 7, 996–1005 (1997).
    Article CAS Google Scholar
  4. Shen, P. et al. Population genetic implications from sequence variation in four Y chromosome genes. Proc. Natl Acad. Sci. USA 97, 7354–7359 (2000).
    Article CAS Google Scholar
  5. Hammer, M.F. et al. Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol. Biol. Evol. 15, 427–441 (1998).
    Article CAS Google Scholar
  6. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism Genetics 123, 585–595 (1989).
    CAS Google Scholar
  7. Nachman, M.W. Y chromosome variation of mice and men. Mol. Biol. Evol. 15, 1744–1750 (1998).
    CAS Google Scholar
  8. Jaruzelska, J., Zietkiewicz, E. & Labuda, D. Is selection responsible for the low level of variation in the last intron of the ZFY locus? Mol. Biol. Evol. 16, 1633–1640 (1999).
    Article CAS Google Scholar
  9. Wyckoff, G.J., Wang, W. & Wu, C.I. Rapid evolution of male reproductive genes in the descent of man. Nature 403, 304–309 ( 2000).
    Article CAS Google Scholar
  10. Jorde, L.B. et al. The distribution of human genetic diversity: a comparison of mitochondrial, autosomal, and Y-chromosome data. Am. J. Hum. Genet. 66, 979–988 ( 2000).
    Article CAS Google Scholar
  11. Thomson, R. et al. Recent common ancestry of human Y chromosomes: Evidence from DNA sequence data. Proc. Natl Acad. Sci. USA 97, 7360–7365 (2000).
    Article CAS Google Scholar
  12. Pritchard, J.K., Seielstad, M.T., Perez-Lezaun, A. & Feldman, M.W. Population growth of human Y chromosomes: a study of Y chromosome microsatellites. Mol. Biol. Evol. 16, 1791–1798 (1999).
    Article CAS Google Scholar
  13. Klein, R.G. The Human Career: Human Biological and Cultural Origins (University of Chicago Press, Illinois, 1999).
    Google Scholar
  14. Quintana-Murci, L. et al. Genetic evidence of an early exit of Homo sapiens sapiens from Africa through eastern Africa. Nature Genet. 23 , 437–441 (1999).
    Article CAS Google Scholar
  15. Rogers, A.R. Genetic evidence for a Pleistocene population explosion. Evolution 49, 608–615 ( 1995).
    Article Google Scholar
  16. Vollrath, D. et al. The human Y chromosome: a 43-interval map based on naturally occurring deletions. Science 258, 52– 59 (1992).
    Article CAS Google Scholar
  17. Hammer, M.F. & Horai, S. Y chromosomal DNA variation and the peopling of Japan. Am. J. Hum. Genet. 56, 951–962 (1995).
    CAS Google Scholar
  18. Seielstad, M.T. et al. Construction of human Y-chromosome haplotypes using a new polymorphic A to G transition. Hum. Mol. Genet. 3, 2159–2161 (1994).
    Article CAS Google Scholar
  19. Hammer, M.F. et al. The geographic distribution of human Y chromosome variation . Genetics 145, 787–805 (1997).
    CAS Google Scholar
  20. Zerjal, T. et al. Genetic relationships of Asians and northern Europeans, revealed by Y-chromosomal DNA analysis. Am. J. Hum. Genet. 60 , 1174–1183 (1997).
    CAS Google Scholar
  21. Bergen, A.W. et al. An Asian-native American paternal lineage identified by RPS4Y resequencing and by microsatellite haplotyping. Ann. Hum Genet. 63, 63–80 ( 1999).
    Article CAS Google Scholar
  22. Bianchi, N.O. et al. Origin of Amerindian Y-chromosomes as inferred by the analysis of six polymorphic markers. Am. J. Phys. Anthropol. 102, 79–89 (1997).
    Article CAS Google Scholar
  23. Diamond, J. Guns, Germs, and Steel (Norton, New York, 1999).
    Google Scholar
  24. Macaulay, V. et al. The emerging tree of west Eurasian mtDNAs: a synthesis of control-region sequences and RFLPs. Am. J. Hum. Genet. 64, 232–249 (1999).
    Article CAS Google Scholar
  25. Jin, L. et al. Distribution of haplotypes from a chromosome 21 region distinguishes multiple prehistoric human migrations. Proc. Natl Acad. Sci. USA 96, 3796–3800 ( 1999).
    Article CAS Google Scholar
  26. Cavalli-Sforza, L.L., Menozzi, P. & Piazza, A. The History and Geography of Human Genes (Princeton University Press, Princeton, New Jersey, 1994).
    Google Scholar

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Acknowledgements

We thank the 1,062 men who donated DNA; R.G. Klein, J. Mountain and M. Ruhlen for helpful discussions; D. Vollrath, R. Hyman and F.S. Dietrich for Y-specific cosmid sequences; and J. Block, D. Soergel, K. Prince, C. Edmonds and A. Rojas for technical help. A.W. Bergen made the RPS4YC711T marker (M130) information available to us before its publication. This work was supported in part by the NIH, NIHGR and L.S.B. Leakey Foundation.

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Authors and Affiliations

  1. Department of Genetics, Stanford University, Stanford, California, USA
    Peter A. Underhill, Alice A. Lin, Giuseppe Passarino & L. Luca Cavalli-Sforza
  2. Stanford DNA Sequencing and Technology Center, Palo Alto, California, USA
    Peidong Shen, Wei H. Yang, Erin Kauffman, Ronald W. Davis & Peter. J. Oefner
  3. University of Texas-Houston, Human Genetics Center, Houston, Texas, USA
    Li Jin
  4. Sackler Faculty of Medicine, Human Genetics, Tel-Aviv University, Tel-Aviv, Israel
    Batsheva Bonné-Tamir
  5. Unitat de Biologia Evolutiva, Facultat de Ciències de la Salut i de la Vida, Universitat Pompeu Fabra, Barcelona, Catalonia, Spain
    Jaume Bertranpetit
  6. Dipartimento di Zoologia e Antropologia Biologica, Università di Sassari, Sassari, Italy
    Paolo Francalacci
  7. Institute of Endemic Diseases, University of Khartoum, Sudan
    Muntaser Ibrahim
  8. Department of Human Genetics, School of Pathology, South African Institute for Medical Research and the University of Witwatersrand, Johannesburg, South Africa
    Trefor Jenkins
  9. Department of Genetics, Yale University School of Medicine, New Haven, Connecticut, USA
    Judith R. Kidd
  10. Dr. A. Q. Khan Research Laboratories, Biomedical & Genetic Engineering Laboratories, Islamabad, Pakistan
    S. Qasim Mehdi
  11. Harvard School of Public Health, Program for Population Genetics, Boston, Massachusetts, USA
    Mark T. Seielstad
  12. Wellcome Trust Centre for Human Genetics, University of Oxford, Headington, UK
    R. Spencer Wells
  13. Department of Genetics, Department of Genetics, Biology and Biochemistry, University of Torino, Torino, Italy
    Alberto Piazza
  14. Department of Biological Sciences, Herrin Laboratories, Stanford University, California, USA
    Marcus W. Feldman

Authors

  1. Peter A. Underhill
  2. Peidong Shen
  3. Alice A. Lin
  4. Li Jin
  5. Giuseppe Passarino
  6. Wei H. Yang
  7. Erin Kauffman
  8. Batsheva Bonné-Tamir
  9. Jaume Bertranpetit
  10. Paolo Francalacci
  11. Muntaser Ibrahim
  12. Trefor Jenkins
  13. Judith R. Kidd
  14. S. Qasim Mehdi
  15. Mark T. Seielstad
  16. R. Spencer Wells
  17. Alberto Piazza
  18. Ronald W. Davis
  19. Marcus W. Feldman
  20. L. Luca Cavalli-Sforza
  21. Peter. J. Oefner

Corresponding author

Correspondence toPeter A. Underhill.

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Underhill, P., Shen, P., Lin, A. et al. Y chromosome sequence variation and the history of human populations.Nat Genet 26, 358–361 (2000). https://doi.org/10.1038/81685

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