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Conservation of Y-linked genes during human evolution revealed by comparative sequencing in chimpanzee

  • 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.

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References

  1. 1

    Aitken, R. J. & Marshall Graves, J. A. The future of sex. Nature 415, 963 (2002)

  2. 2

    Graves, J. A. The degenerate Y chromosome—can conversion save it? Reprod. Fertil. Dev. 16, 527–534 (2004)

  3. 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)

  4. 4

    Rozen, S. et al. Abundant gene conversion between arms of palindromes in human and ape Y chromosomes. Nature 423, 873–876 (2003)

  5. 5

    Lahn, B. T. & Page, D. C. Four evolutionary strata on the human X chromosome. Science 286, 964–967 (1999)

  6. 6

    Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Phil. Trans. R. Soc. Lond. B 355, 1563–1572 (2000)

  7. 7

    Watanabe, H. et al. DNA sequence and comparative analysis of chimpanzee chromosome 22. Nature 429, 382–388 (2004)

  8. 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)

  9. 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)

  10. 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)

  11. 11

    Hellmann, I. et al. Selection on human genes as revealed by comparisons to chimpanzee cDNA. Genome Res. 13, 831–837 (2003)

  12. 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)

  13. 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)

  14. 14

    Rice, W. R. Genetic hitchhiking and the evolution of reduced genetic activity of the Y sex chromosome. Genetics 116, 161–167 (1987)

  15. 15

    Lahn, B. T. & Page, D. C. Functional coherence of the human Y chromosome. Science 278, 675–680 (1997)

  16. 16

    Parker, G. A. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525–567 (1970)

  17. 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)

  18. 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)

  19. 19

    Dixson, A. F. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings (Univ. Chicago Press, Chicago, 1998)

  20. 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)

  21. 21

    Tilford, C. A. et al. A physical map of the human Y chromosome. Nature 409, 943–945 (2001)

  22. 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)

  23. 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)

  24. 24

    Kumar, S., Tamura, K., Jakobsen, I. B. & Nei, M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245 (2001)

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Acknowledgements

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

Author information

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.

Correspondence to David C. Page.

Supplementary information

  1. Supplementary Figures

    This file contains Supplementary Figures S1-S9. (PDF 3570 kb)

  2. Supplementary Tables

    This file contains Supplementary Tables S1-S6. (PDF 242 kb)

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Further reading

Figure 1: Dot-plot comparison of the X-degenerate region of the chimpanzee Y chromosome (below) with the euchromatic region of the human Y chromosome (left).
Figure 2: Human–chimpanzee divergence in coding sequence and introns of X-degenerate genes and pseudogenes.
Figure 3: Lengths of coding sequences of X-degenerate genes on chimpanzee and human Y chromosomes, and their human X-linked homologues.

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