Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee (original) (raw)

Nature volume 437, pages 100–103 (2005)Cite this article

A Corrigendum to this article was published on 11 May 2006

Abstract

The human Y chromosome, transmitted clonally through males, contains far fewer genes than the sexually recombining autosome from which it evolved. The enormity of this evolutionary decline has led to predictions that the Y chromosome will be completely bereft of functional genes within ten million years1,2. Although recent evidence of gene conversion within massive Y-linked palindromes runs counter to this hypothesis, most unique Y-linked genes are not situated in palindromes and have no gene conversion partners3,4. The ‘impending demise’ hypothesis thus rests on understanding the degree of conservation of these genes. Here we find, by systematically comparing the DNA sequences of unique, Y-linked genes in chimpanzee and human, which diverged about six million years ago, evidence that in the human lineage, all such genes were conserved through purifying selection. In the chimpanzee lineage, by contrast, several genes have sustained inactivating mutations. Gene decay in the chimpanzee lineage might be a consequence of positive selection focused elsewhere on the Y chromosome and driven by sperm competition.

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. Aitken, R. J. & Marshall Graves, J. A. The future of sex. Nature 415, 963 (2002)
    Article ADS CAS PubMed Google Scholar
  2. Graves, J. A. The degenerate Y chromosome—can conversion save it? Reprod. Fertil. Dev. 16, 527–534 (2004)
    Article PubMed Google Scholar
  3. Skaletsky, H. et al. The male-specific region of the human Y chromosome is a mosaic of discrete sequence classes. Nature 423, 825–837 (2003)
    Article ADS CAS PubMed Google Scholar
  4. Rozen, S. et al. Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423, 873–876 (2003)
    Article ADS CAS PubMed Google Scholar
  5. Lahn, B. T. & Page, D. C. Four evolutionary strata on the human X chromosome. Science 286, 964–967 (1999)
    Article CAS PubMed Google Scholar
  6. Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Phil. Trans. R. Soc. Lond. B 355, 1563–1572 (2000)
    Article CAS Google Scholar
  7. Watanabe, H. et al. DNA sequence and comparative analysis of chimpanzee chromosome 22. Nature 429, 382–388 (2004)
    Article ADS CAS PubMed Google Scholar
  8. Miyata, T., Hayashida, H., Kuma, K., Mitsuyasu, K. & Yasunaga, T. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harb. Symp. Quant. Biol. 52, 863–867 (1987)
    Article CAS PubMed Google Scholar
  9. Yeh, R. F., Lim, L. P. & Burge, C. B. Computational inference of homologous gene structures in the human genome. Genome Res. 11, 803–816 (2001)
    Article CAS PubMed PubMed Central Google Scholar
  10. Altschul, 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 CAS PubMed Google Scholar
  11. Hellmann, I. et al. Selection on human genes as revealed by comparisons to chimpanzee cDNA. Genome Res. 13, 831–837 (2003)
    Article CAS PubMed PubMed Central Google Scholar
  12. Casane, D., Boissinot, S., Chang, B. H., Shimmin, L. C. & Li, W. Mutation pattern variation among regions of the primate genome. J. Mol. Evol. 45, 216–226 (1997)
    Article ADS CAS PubMed Google Scholar
  13. Sun, C. et al. An azoospermic man with a de novo point mutation in the Y-chromosomal gene USP9Y. Nature Genet. 23, 429–432 (1999)
    Article CAS PubMed Google Scholar
  14. Rice, W. R. Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116, 161–167 (1987)
    CAS PubMed PubMed Central Google Scholar
  15. Lahn, B. T. & Page, D. C. Functional coherence of the human Y chromosome. Science 278, 675–680 (1997)
    Article ADS CAS PubMed Google Scholar
  16. Parker, G. A. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525–567 (1970)
    Article Google Scholar
  17. Dorus, S., Evans, P. D., Wyckoff, G. J., Choi, S. S. & Lahn, B. T. Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nature Genet. 36, 1326–1329 (2004)
    Article CAS PubMed Google Scholar
  18. 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
  19. Dixson, A. F. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings (Univ. Chicago Press, Chicago, 1998)
    Google Scholar
  20. Filatov, D. A., Moneger, F., Negrutiu, I. & Charlesworth, D. Low variability in a Y-linked plant gene and its implications for Y-chromosome evolution. Nature 404, 388–390 (2000)
    Article ADS CAS PubMed Google Scholar
  21. Tilford, C. A. et al. A physical map of the human Y chromosome. Nature 409, 943–945 (2001)
    Article ADS CAS PubMed Google Scholar
  22. Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994)
    Article CAS PubMed PubMed Central Google Scholar
  23. Whitfield, L. S., Lovell-Badge, R. & Goodfellow, P. N. Rapid sequence evolution of the mammalian sex-determining gene SRY. Nature 364, 713–715 (1993)
    Article ADS CAS PubMed Google Scholar
  24. Kumar, S., Tamura, K., Jakobsen, I. B. & Nei, M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245 (2001)
    Article CAS PubMed Google Scholar

Download references

Acknowledgements

This work was supported by the National Institutes of Health and the Howard Hughes Medical Institute.

Author information

Authors and Affiliations

  1. Howard Hughes Medical Institute, Whitehead Institute,
    Jennifer F. Hughes, Helen Skaletsky, Tatyana Pyntikova, Steve Rozen & David C. Page
  2. Department of Biology, Massachusetts Institute of Technology, 9 Cambridge Center, Cambridge, Massachusetts, 02142, USA
    Jennifer F. Hughes, Helen Skaletsky, Tatyana Pyntikova, Steve Rozen & David C. Page
  3. Genome Sequencing Center, Washington University School of Medicine, 4444 Forest Park Boulevard, Missouri, 63108, St Louis, USA
    Patrick J. Minx, Tina Graves & Richard K. Wilson

Authors

  1. Jennifer F. Hughes
    You can also search for this author inPubMed Google Scholar
  2. Helen Skaletsky
    You can also search for this author inPubMed Google Scholar
  3. Tatyana Pyntikova
    You can also search for this author inPubMed Google Scholar
  4. Patrick J. Minx
    You can also search for this author inPubMed Google Scholar
  5. Tina Graves
    You can also search for this author inPubMed Google Scholar
  6. Steve Rozen
    You can also search for this author inPubMed Google Scholar
  7. Richard K. Wilson
    You can also search for this author inPubMed Google Scholar
  8. David C. Page
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toDavid C. Page.

Ethics declarations

Competing interests

GenBank accession numbers for CERV1 and CERV2 are AY692036 and AY692037, respectively. GenBank accession numbers for all complementary DNA sequences are listed in Supplementary Table 5; accession numbers for all BAC and fosmid clones are listed in Supplementary Table 6. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Rights and permissions

About this article

Cite this article

Hughes, J., Skaletsky, H., Pyntikova, T. et al. Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee.Nature 437, 100–103 (2005). https://doi.org/10.1038/nature04101

Download citation

Editorial Summary

The chimpanzee genome

The cover photo by Kevin Langergraber shows the adult female chimpanzee ‘Jolie’ in Kibale National Park, Uganda. This was taken on 16 August 2004, a few weeks before Jolie gave birth to her first infant. This week marks a landmark in the study of our closest living relative: the publication by the Chimpanzee Sequencing and Analysis Consortium of the initial sequence of the chimpanzee genome, together with a comparison with the human genome. The paper describes changes that have shaped human and chimpanzee species since the split from our common ancestor, and hints at what makes us uniquely human: 35 million single-nucleotide substitutions, 5 million small insertions and deletions, local rearrangements and a chromosome fusion. A comparison of gene duplications in chimpanzee and human genomes reveals gene expression differences that may underlie disease susceptibility. A study of primate genomes shows that subtelomeres are hot spots of recent chromosomal duplication and gene conversion. Conservation of Y-linked genes during human evolution is revealed by comparative sequencing in the chimpanzee. The final research paper in this collection fills a big gap in our knowledge: the first chimpanzee fossils ever found show that chimps and early humans inhabited the same environments in which they evolved and diverged. The fossils — three teeth — are from half-million-year-old sediments in Kenya that also yielded fossils of Homo. Four Progress reviews accompany these papers, looking at chimp culture, social behaviour, psychology and cognition. Elsewhere in the issue, researchers talk about working with chimpanzees, a feature summarizes other primate genome projects, and in two Commentaries, important ethical issues surrounding research on great apes are considered.