Positive selection of a gene family during the emergence of humans and African apes (original) (raw)

Nature volume 413, pages 514–519 (2001)Cite this article

Abstract

Gene duplication followed by adaptive evolution is one of the primary forces for the emergence of new gene function1. Here we describe the recent proliferation, transposition and selection of a 20-kilobase (kb) duplicated segment throughout 15 Mb of the short arm of human chromosome 16. The dispersal of this segment was accompanied by considerable variation in chromosomal-map location and copy number among hominoid species. In humans, we identified a gene family (morpheus) within the duplicated segment. Comparison of putative protein-encoding exons revealed the most extreme case of positive selection among hominoids. The major episode of enhanced amino-acid replacement occurred after the separation of human and great-ape lineages from the orangutan. Positive selection continued to alter amino-acid composition after the divergence of human and chimpanzee lineages. The rapidity and bias for amino-acid-altering nucleotide changes suggest adaptive evolution of the morpheus gene family during the emergence of humans and African apes. Moreover, some genes emerge and evolve very rapidly, generating copies that bear little similarity to their ancestral precursors. Consequently, a small fraction of human genes may not possess discernible orthologues within the genomes of model organisms.

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

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

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

Additional access options:

Similar content being viewed by others

References

  1. Ohno, S. Evolution by Gene Duplication (Springer, Berlin, 1970).
    Book Google Scholar
  2. Stallings, R., Whitmore, S., Doggett, N. & Callen, D. Refined physical mapping of chromosome 16-specific low-abundance repetitive DNA sequences. Cytogenet. Cell Genet. 63, 97–101 (1993).
    Article CAS PubMed Google Scholar
  3. Loftus, B. et al. Genome duplications and other features in 12 Mbp of DNA sequence from human chromosome 16p and 16q. Genomics 60, 295–308 (1999).
    Article CAS PubMed Google Scholar
  4. The International Human Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, 860–920 (2001).
    Article Google Scholar
  5. Bailey, J. A., Yavor, A. M., Massa, H. F., Trask, B. J. & Eichler, E. E. Segmental duplications: organization and impact within the current human genome project assembly. Genome Res. 11, 1005–1017 (2001).
    Article CAS PubMed PubMed Central Google Scholar
  6. Goodman, M. The genomic record of humankind's evolutionary roots. Am. J. Hum. Genet. 64, 31–39 (1999).
    Article CAS PubMed PubMed Central Google Scholar
  7. Li, W. Molecular Evolution (Sinauer, Sunderland, 1997).
    Google Scholar
  8. 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 ADS CAS PubMed Google Scholar
  9. Nurminsky, D. I., Nurminskaya, M. V., De Aguiar, D. & Hartl, D. L. Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396, 572–575 (1998).
    Article ADS CAS PubMed Google Scholar
  10. Duda, T. F. & Palumbi, S. R. Molecular genetics of ecological diversification: duplication and rapid evolution of toxin genes of the venomous gastropod Conus. Proc. Natl Acad. Sci. USA 96, 6820–6823 (1999).
    Article ADS CAS PubMed PubMed Central Google Scholar
  11. Vacquier, V. D., Swanson, W. J. & Lee, Y. H. Positive Darwinian selection on two homologous fertilization proteins: what is the selective pressure driving their divergence? J. Mol. Evol. 44, S15–S22 (1997).
    Article ADS CAS PubMed Google Scholar
  12. Zhang, J., Rosenberg, H. F. & Nei, M. Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc. Natl Acad. Sci. USA 95, 3708–3713 (1998).
    Article ADS CAS PubMed PubMed Central Google Scholar
  13. Hughes, A. L. & Nei, M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335, 167–170 (1988).
    Article ADS CAS PubMed Google Scholar
  14. Messier, W. & Stewart, C. B. Episodic adaptive evolution of primate lysozymes. Nature 385, 151–154 (1997).
    Article ADS CAS PubMed Google Scholar
  15. Ting, C. T., Tsaur, S. C., Wu, M. L. & Wu, C. I. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science 282, 1501–1504 (1998).
    Article CAS PubMed Google Scholar
  16. Davis, L. I. & Blobel, G. Identification and characterization of a nuclear pore complex protein. Cell 45, 699–709 (1986).
    Article CAS PubMed Google Scholar
  17. Horvath, J., Schwartz, S. & Eichler, E. The mosaic structure of a 2p11 pericentromeric segment: A strategy for characterizing complex regions of the human genome. Genome Res. 10, 839–852 (2000).
    Article CAS PubMed PubMed Central Google Scholar
  18. Lichter, P. et al. High-resolution mapping of human chromosome 11 by in situ hybridization with cosmid clones. Science 247, 64–69 (1990).
    Article ADS CAS PubMed Google Scholar
  19. Jukes, T. H. & Cantor, C. R. in Mammalian Protein Metabolism (ed. Munro, H. N.) 21–123 (Academic, New York, 1969).
    Book Google Scholar
  20. Tajima, F. Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135, 599–607 (1993).
    CAS PubMed PubMed Central Google Scholar
  21. Nei, M. & Gojobori, T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418–426 (1986).
    CAS PubMed Google Scholar
  22. Nei, M. & Kumar, S. Molecular Evolution and Phylogenetics (Oxford Univ. Press, New York, 2000).
    Google Scholar

Download references

Acknowledgements

We thank W. E. Kutz and D. Zivkovic for technical assistance and sequencing analyses. This work was supported by grants from the National Institutes of Health and the US Department of Energy to E.E.E., and grants from Progretti di Interesse Nationale (PRIN), Centro Eccelenza (CE), Ministero per la Ricerca Scientifica e Tecnologica (MURST) and Telethon to M.R. We are grateful to C. I. Wu, A. Chakravarti, D. Cutler, D. Locke, G. Matera and H. Willard for comments on this manuscript.

Author information

Authors and Affiliations

  1. Department of Genetics and Center for Human Genetics, Case Western Reserve University School of Medicine and University Hospitals of Cleveland, Cleveland, 44106, Ohio, USA
    Matthew E. Johnson, Jeffrey A. Bailey & Evan E. Eichler
  2. DAPEG, Sezione di Genetica, Via Amendola 165/A, Bari, 70126, Italy
    Luigi Viggiano & Mariano Rocchi
  3. Section of Molecular Carcinogenesis, Institute of Cancer Research, Haddow Laboratories, 15 Cotswold Road, Sutton, MS2 5NG, Surrey, UK
    Munah Abdul-Rauf & Graham Goodwin

Authors

  1. Matthew E. Johnson
    You can also search for this author inPubMed Google Scholar
  2. Luigi Viggiano
    You can also search for this author inPubMed Google Scholar
  3. Jeffrey A. Bailey
    You can also search for this author inPubMed Google Scholar
  4. Munah Abdul-Rauf
    You can also search for this author inPubMed Google Scholar
  5. Graham Goodwin
    You can also search for this author inPubMed Google Scholar
  6. Mariano Rocchi
    You can also search for this author inPubMed Google Scholar
  7. Evan E. Eichler
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toEvan E. Eichler.

Supplementary information

Rights and permissions

About this article

Cite this article

Johnson, M., Viggiano, L., Bailey, J. et al. Positive selection of a gene family during the emergence of humans and African apes.Nature 413, 514–519 (2001). https://doi.org/10.1038/35097067

Download citation