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.
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References
Eberhard, W. G. Sexual Selection and Animal Genitalia (Harvard Univ. Press, Cambridge, MA, 1985).
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).
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).
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).
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).
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).
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).
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).
Sutton, K. A. & Wilkinson, M. F. Rapid evolution of a homeodomain: evidence for positive selection. J. Mol. Evol. 45, 579–588 (1997).
Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, 1983).
Darwin, C. The Descent of Man and Selection in Relation to Sex (D. Appleton, New York, 1871).
McDonald, J. & Kreitman, M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–654 (1991).
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).
Yang, Z., Nielson, R. & Hasegawa, M. Models of amino acid substitution and applications to mitochondrial protein evolution. Mol. Biol. Evol. 15 , 1600–1611 (1998).
Nelson, J. E. & Krawetz, S. A. Linkage of human spermatid-specific basic nuclear protein genes. J. Biol. Chem. 268, 2932–2936 (1993).
Gould, K. G. Scanning electron microscopy of the primate sperm. Intl Rev. Cytol. 63, 323–255 ( 1980).
Retief, J. D. et al. Evolution of protamine P1 gene in primates. J. Mol. Evol. 37, 426–434 ( 1993).
Retief, J. D. & Dixon, G. H. Evolution of pro-protamine P2 genes in primates. Eur. J. Biochem. 214, 609– 615 (1993).
Dixson, A. F. Primate Sexuality (Oxford Univ. Press, 1998).
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).
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).
Li, W. -H. Molecular Evolution (Sinauer, Sunderland, MA, 1997).
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).
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).
Queralt, R. et al. Direct sequencing of the human protamine P1 gene and application in forensic medicine. J. Forensic Sci. 38, 1491–1501 (1993).
Grantham, R. Amino acid difference formula to help explain protein evolution. Science 185, 862–864 ( 1974).
Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon, Oxford, 1930).
Shimmin, L. C., Chang, B. H. -J. & Li, W. -H. Male-driven evolution of DNA sequences. Nature 362, 745– 747 ( 1993).
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).
Li, W. -H. Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J. Mol. Evol. 36, 96–99 (1993).
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.
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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
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DOI: https://doi.org/10.1038/35002070
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