Abstract
For over 30 years a central question in molecular evolution has been whether natural selection plays a substantial role in evolution at the DNA sequence level1,2. Evidence has accumulated over the last decade that adaptive evolution does occur at the protein level3,4, but it has remained unclear how prevalent adaptive evolution is. Here we present a simple method by which the number of adaptive substitutions can be estimated and apply it to data from Drosophila simulans and D. yakuba. We estimate that 45% of all amino-acid substitutions have been fixed by natural selection, and that on average one adaptive substitution occurs every 45 years in these species.
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References
Gillespie, J. H. The Causes of Molecular Evolution (Oxford Univ. Press, Oxford, 1991).
Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983).
Kreitman, M. & Akashi, H. Molecular evidence for natural selection. Annu. Rev. Ecol. Syst. 26, 403–422 (1995).
Yang, Z. & Bielawski, J. P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496–503 (2000).
Charlesworth, B. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet. Res. 63, 213–227 (1994).
Fay, J., Wycoff, G. J. & Wu, C.-I. Positive and negative selection on the human genome. Genetics 158, 1227–1234 (2001).
McDonald, J. H. & Kreitman, M. Adaptive evolution at the Adh locus in Drosophila. Nature 351, 652–654 (1991).
Charlesworth, B., Morgan, M. T. & Charlesworth, D. The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303 (1993).
Maynard Smith, J. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23–35 (1974).
Begun, D. J. & Aquadro, C. F. levels of naturally occuring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519–520 (1992).
Begun, D. The frequency distribution of nucleotide variation in Drosophila simulans. Mol. Biol. Evol. 18, 1343–1352 (2001).
Kliman, R. Recent selection on synonymous codon usage in Drosophila. J. Mol. Evol. 49, 343–351 (1999).
Adams, M. D. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185–2195 (2000).
Powell, J. R. & DeSalle, R. Drosophila molecular phylogenies and their uses. Evol. Biol. 28, 87–138 (1995).
Haldane, J. B. S. The cost of natural selection. J. Genet. 55, 511–524 (1957).
Kimura, M. Evolutionary rate at the molecular level. Nature 217, 624–626 (1968).
Thompson, J. D., Higgins, D. G. & Gibson, T. J. ClustalW—improving the sensitivity of progressive multiple alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673–4680 (1994).
Xia, X. Data Analysis in Molecular Biology and Evolution (Kluwer Academic, London, 2000).
Rozas, J. & Rozas, R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175 (1999).
Yang, Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555–556 (1997).
Acknowledgements
We thank B. Charlesworth, C.-I. Wu, S. Otto, M. Whitlock, T. Johnson, P. Awadalla, J. Gillespie, G. McVean and P. Keightley for helpful discussions, and E. Moriyama for help with data collection. N.G.C.S. was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) and A.E.-W. is funded by the Royal Society and the BBSRC.
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Smith, N., Eyre-Walker, A. Adaptive protein evolution in Drosophila. Nature 415, 1022–1024 (2002). https://doi.org/10.1038/4151022a
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DOI: https://doi.org/10.1038/4151022a
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