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:

Rapid evolution of male reproductive genes in the descent of man

Abstract

A diverse body of morphological and genetic evidence has suggested that traits pertaining to male reproduction may have evolved much more rapidly than other types of character1,2,3. Recently, DNA sequence comparisons have also shown a very high level of divergence in male reproductive proteins between closely related Drosophila species4,5,6, among marine invertebrates7,8 and between mouse and rat9. Here we show that rapid evolution of male reproductive genes is observable in primates and is quite notable in the lineages to human and chimpanzee. Nevertheless, rapid evolution by itself is not necessarily an indication of positive darwinian selection; relaxation of negative selection is often equally compatible with the DNA sequence data. By taking three statistical approaches, we show that positive darwinian selection is often the driving force behind this rapid evolution. These results open up opportunities to test the hypothesis that sexual selection plays some role in the molecular evolution of higher primates.

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

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

Figure 1: Evolution of the protamine gene complex.
Figure 2: Observed and simulated numbers of nucleotide changes.
Figure 3: Observed and simulated numbers of nucleotide changes.

Similar content being viewed by others

References

  1. Eberhard, W. G. Sexual Selection and Animal Genitalia (Harvard Univ. Press, Cambridge, MA, 1985).

    Book  Google Scholar 

  2. Coulthart, M. B. & Singh, R. S. Low genic variation in male reproductive tract proteins of Drosophila melanogaster and Drosophila simulans. Mol. Biol. Evol. 5, 167–181 (1988).

    CAS  Google Scholar 

  3. Wu, C. I., Johnson, N. A. & Palopoli, M. F. Haldane's rule and its legacy: why are there so many sterile males. Trends Ecol. Evol. 11, 281 –284 (1996).

    Article  CAS  Google Scholar 

  4. Tsaur, S., Ting, C. T. & Wu, C. -I. Positive selection driving the evolution of a gene of male reproduction, ACP26Aa of Drosophila: II Divergence vs. polymorphism. Mol. Biol. Evol. 15, 1040–1046 ( 1998).

    Article  CAS  Google Scholar 

  5. Ting, C., 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  Google Scholar 

  6. Nurminsky, D. I., Nurminskaya, M. V., Aguiar, D. D. & Hartl, D. L. Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396, 572–575 (1998).

    Article  ADS  CAS  Google Scholar 

  7. Lee, Y., Ohta, T. & Vacquier, V. D. Positive selection is a general phenomena in the evolution of abalone sperm lysin. Mol. Biol. Evol. 6, 424–435 (1995).

    Google Scholar 

  8. Metz, E. C. & Palumbi, S. R. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13, 397– 406 (1996).

    Article  CAS  Google Scholar 

  9. Sutton, K. A. & Wilkinson, M. F. Rapid evolution of a homeodomain: evidence for positive selection. J. Mol. Evol. 45, 579–588 (1997).

    Article  ADS  CAS  Google Scholar 

  10. Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, 1983).

    Book  Google Scholar 

  11. Darwin, C. The Descent of Man and Selection in Relation to Sex (D. Appleton, New York, 1871).

    Google Scholar 

  12. McDonald, J. & Kreitman, M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654 (1991).

    Article  ADS  CAS  Google Scholar 

  13. Li, W. -H., Wu, C. I. & Luo, C. C. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol. Biol. Evol. 2, 150 –174 (1985).

    Google Scholar 

  14. Yang, Z., Nielson, R. & Hasegawa, M. Models of amino acid substitution and applications to mitochondrial protein evolution. Mol. Biol. Evol. 15 , 1600–1611 (1998).

    Article  CAS  Google Scholar 

  15. Nelson, J. E. & Krawetz, S. A. Linkage of human spermatid-specific basic nuclear protein genes. J. Biol. Chem. 268, 2932–2936 (1993).

    CAS  Google Scholar 

  16. Gould, K. G. Scanning electron microscopy of the primate sperm. Intl Rev. Cytol. 63, 323–255 ( 1980).

    Article  CAS  Google Scholar 

  17. Retief, J. D. et al. Evolution of protamine P1 gene in primates. J. Mol. Evol. 37, 426–434 ( 1993).

    Article  ADS  CAS  Google Scholar 

  18. Retief, J. D. & Dixon, G. H. Evolution of pro-protamine P2 genes in primates. Eur. J. Biochem. 214, 609– 615 (1993).

    Article  CAS  Google Scholar 

  19. Dixson, A. F. Primate Sexuality (Oxford Univ. Press, 1998).

    Google Scholar 

  20. Sillen-Tullberg, B. & Moller, A. P. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. Am. Nat. 141, 1– 25 (1993).

    Article  CAS  Google Scholar 

  21. Rooney, A. P. & Zhang, J. Rapid evolution of a primate sperm protein: relaxation of functional constraint or positive Darwinian selection. Mol. Biol. Evol. 16, 706– 710 (1999).

    Article  CAS  Google Scholar 

  22. Li, W. -H. Molecular Evolution (Sinauer, Sunderland, MA, 1997).

    Google Scholar 

  23. Maeda, N., Wu, C-I, Bliska, J. & Reneke, J. Molecular evolution of intergenic DNA in higher primates: patterns of DNA changes, molecular clock and evolution of repetitive sequences. Mol. Biol. Evol. 5, 1–20 (1988).

    CAS  Google Scholar 

  24. Schlicker, M., Schnulle, V., Schneppel, L., Vorob, V. I. & W. Engel, W. Disturbances of nuclear condensation in human spermatozoa: search for mutations in the genes of protamine 1, protamine 2 and transitional protein 1. Hum. Reprod. 9, 2313–2317 (1994).

    Article  CAS  Google Scholar 

  25. Queralt, R. et al. Direct sequencing of the human protamine P1 gene and application in forensic medicine. J. Forensic Sci. 38, 1491–1501 (1993).

    Article  CAS  Google Scholar 

  26. Grantham, R. Amino acid difference formula to help explain protein evolution. Science 185, 862–864 ( 1974).

    Article  ADS  CAS  Google Scholar 

  27. Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, Oxford, 1930).

    Book  Google Scholar 

  28. Shimmin, L. C., Chang, B. H. -J. & Li, W. -H. Male-driven evolution of DNA sequences. Nature 362, 745– 747 ( 1993).

    Article  ADS  CAS  Google Scholar 

  29. Li, W. -H., Wu, C. -I & Luo, C. C. Nonrandomness of point mutations as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. J. Mol. Evol. 21, 58–71 (1984).

    Article  ADS  CAS  Google Scholar 

  30. Li, W. -H. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36, 96–99 (1993).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Ober, C. Grimsley, C. Toomajian and P. Parham for generously providing DNA samples. We are very grateful to I. Boussy, J. Fay, M. Jensen, D. Ledbetter, W.-H. Li, M. Long and C.-T. Ting for comments on earlier drafts and to S.-C. Tsaur, J. Gladstone and M.-L. Wu for technical assistance and advice. This work was supported by NIH and NSF grants to C.I.W.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chung-I Wu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wyckoff, G., Wang, W. & Wu, CI. Rapid evolution of male reproductive genes in the descent of man. Nature 403, 304–309 (2000). https://doi.org/10.1038/35002070

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35002070

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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