Abstract
Assuming that new mutations arise mainly during DNA replication, sequence evolution in mammals has been seen as ‘male driven’ (ref. 1) because of the many more cell divisions in spermatogenesis than in oogenesis. Molecular support for this idea has been obtained from the observation of higher substitution rates in genes on the Y than on the X chromosome of primates and rodents2–4, which are species with male heterogamety, but has not been confirmed by the reciprocal analysis of organisms with female heterogamety. The recent suggestion that an intrinsic reduction in the X-chromosome mutation rate may be confounded with male effects in previous comparisons5, and the paradoxical finding of low levels of polymorphism on the primate Y chromosome6–8 indicate that the idea of male-biased mutation rate needs to be re-examined. We have analysed the molecular evolution of the gene CHD, which is present on the Z and W sex chromosomes of birds. The substitution rate at synonymous positions, as well as in intron DNA, was considerably higher on the Z chromosome than on the female-specific W chromosome, with an estimated male-to-female bias in mutation rate (αm) of 3.9–6.5. Thus, evolution appears to be male driven in birds—a situation that supports a neutral model of molecular evolution.
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References
Miyata, T., Hayashida, H., Kuma, K., Mitsuyasa, K. & Yasunaga, T. Male-driven molecular evolution: a model and nucleotide sequence analysis. Cold Spring Harbor Symp. Quant. Biol. 52, 863–867 (1987).
Shimmin, L.C., Chang, B.H.J. & Li, W.-H. Male-driven evolution of DNA sequences. Nature 362, 745–747 (1993).
Shimmin, L.C., Chang, B.H.J. & Li, W.-H. Contrasting rates of nucleotide substitution in the X-linked and Y-linked zinc finger genes. J. Mol. Evol. 39, 569–578 (1994).
Huang, W., Chang, B.H.J., Gu, X., Hewett-Emmett, D. & Li, W.-H. Sex differences in mutation rate in higher primates estimated from AMG intron sequences. J. Mol. Evol. 44, 463–465 (1994).
McVean, G.T. & Hurst, L.D. Evidence for a selectively favourable reduction in the mutation rate of the X-chromosome. Nature 386, 388–392 (1997).
Malaspina, P. et al. The human Y chromosome shows a low level of DNA polymorphism. Ann. Hum. Genet. 54, 297–305 (1990).
Dorit, R.L., Akashi, H. & Gilbert, W. Absence of polymorphism at the ZFY locus in the human Y chromosome. Science 268, 1183–1185 (1995).
Burrows, W. & Ryder, O.A. Y-chromosome variation in great apes. Nature 385, 125–126 (1997).
Ellegren, H. First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proc. R. Soc. Lond B Biol. Sci. 263, 1635–1641 (1996).
Griffiths, R., Daan, S. & Dijkstra, C. Sex identification in birds using two CHD genes. Proc. R. Soc. Lond. B Biol. Sci. 263, 1251–1256 (1996).
Delmas, V., Stokes, D. G. & Perry, R. P. A mammalian DNA-binding protein that contains a chromo-domain and an SNF2/SWI2-like helicase domain. Proc. Natl. Acad. Sci. USA 90, 2414–2418 (1994).
Stokes, D.G. & Perry, R.P. DNA-binding and chromatin localization properties of CHD1. Mol. Cell. Biol. 15, 2745–2753 (1995).
Li, W.-H. & Graur, D. Fundamentals of Molecular Evolution (Sinauer, Sunderland, Massachusetts, 1991).
Wolfe, K.H. & Sharp, P.M. Mammalian gene evolution: nucleotide sequence divergence between mouse and rat. J. Mol. Evol. 37, 441–456 (1993).
Chang, B.H.J., Shimmin, L.C., Shyue, S-K., Hewett-Emmett, D. & Li, W.-H. Weak male-driven molecular evolution in rodents. Proc. Natl. Acad. Sci. USA 91, 827–831 (1994).
Jones, R.C. & Lin, M. Spermatogenesis in birds. Oxf. Rev. Reprod. Biol. 15, 233–260 (1993).
Sibley, C.G. & Ahlquist, J.E. Phylogeny and Classification of Birds: A Study in Molecular Evolution (Yale University Press, New Haven, Connecticut, 1990).
Pamilo, P. & Bianchi, N.O. Evolution of the Zfx and Zfy genes: rates and interdependence between the genes. Mol. Biol. Evol. 10, 271–281 (1993).
Tajima, F. & Nei, M. Estimation of evolutionary distance between nucleotide sequences. Mol. Biol. Evol. 1, 269–285 (1984).
Kumar, S., Tamura, K. & Nei, M. MEGA: Molecular Evolutionary Genetic Analysis, version 1.0 (Pennsylvania State University, University Park, Pennsylvania, 1993).
Li, W.-H. A statistical test of phylogenies estimated from sequence data. Mol. Biol. Evol. 6, 424–435 (1989).
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Ellegren, H., Fridolfsson, AK. Male–driven evolution of DNA sequences in birds. Nat Genet 17, 182–184 (1997). https://doi.org/10.1038/ng1097-182
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DOI: https://doi.org/10.1038/ng1097-182
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