Adaptive protein evolution in Drosophila (original) (raw)

Nature volume 415, pages 1022–1024 (2002)Cite this article

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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Figure 1: The distribution of 1,000 bootstrap values of \(\overline{α}\) for the divergence between Drosophila simulans and D. yakuba for genes in which _P_s > 5.

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References

  1. Gillespie, J. H. The Causes of Molecular Evolution (Oxford Univ. Press, Oxford, 1991).
    Google Scholar
  2. Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983).
    Book Google Scholar
  3. Kreitman, M. & Akashi, H. Molecular evidence for natural selection. Annu. Rev. Ecol. Syst. 26, 403–422 (1995).
    Article Google Scholar
  4. Yang, Z. & Bielawski, J. P. Statistical methods for detecting molecular adaptation. Trends Ecol. Evol. 15, 496–503 (2000).
    Article CAS Google Scholar
  5. Charlesworth, B. The effect of background selection against deleterious mutations on weakly selected, linked variants. Genet. Res. 63, 213–227 (1994).
    Article CAS Google Scholar
  6. Fay, J., Wycoff, G. J. & Wu, C.-I. Positive and negative selection on the human genome. Genetics 158, 1227–1234 (2001).
    CAS PubMed PubMed Central Google Scholar
  7. McDonald, J. H. & Kreitman, M. Adaptive evolution at the Adh locus in Drosophila. Nature 351, 652–654 (1991).
    Article ADS CAS Google Scholar
  8. Charlesworth, B., Morgan, M. T. & Charlesworth, D. The effect of deleterious mutations on neutral molecular variation. Genetics 134, 1289–1303 (1993).
    CAS PubMed PubMed Central Google Scholar
  9. Maynard Smith, J. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23–35 (1974).
    Article Google Scholar
  10. Begun, D. J. & Aquadro, C. F. levels of naturally occuring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356, 519–520 (1992).
    Article ADS CAS Google Scholar
  11. Begun, D. The frequency distribution of nucleotide variation in Drosophila simulans. Mol. Biol. Evol. 18, 1343–1352 (2001).
    Article CAS Google Scholar
  12. Kliman, R. Recent selection on synonymous codon usage in Drosophila. J. Mol. Evol. 49, 343–351 (1999).
    Article ADS CAS Google Scholar
  13. Adams, M. D. et al. The genome sequence of Drosophila melanogaster. Science 287, 2185–2195 (2000).
    Article Google Scholar
  14. Powell, J. R. & DeSalle, R. Drosophila molecular phylogenies and their uses. Evol. Biol. 28, 87–138 (1995).
    Article CAS Google Scholar
  15. Haldane, J. B. S. The cost of natural selection. J. Genet. 55, 511–524 (1957).
    Article Google Scholar
  16. Kimura, M. Evolutionary rate at the molecular level. Nature 217, 624–626 (1968).
    Article ADS CAS Google Scholar
  17. 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).
    Article CAS Google Scholar
  18. Xia, X. Data Analysis in Molecular Biology and Evolution (Kluwer Academic, London, 2000).
    Google Scholar
  19. Rozas, J. & Rozas, R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175 (1999).
    Article CAS Google Scholar
  20. Yang, Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13, 555–556 (1997).
    CAS PubMed Google Scholar

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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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  1. Nick G. C. Smith
    Present address: Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, SE-752 36, Uppsala, Sweden

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  1. Centre for the Study of Evolution and School of Biological Sciences, University of Sussex, Brighton, BN1 9QG, UK
    Nick G. C. Smith & Adam Eyre-Walker

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  1. Nick G. C. Smith
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  2. Adam Eyre-Walker
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Correspondence toAdam Eyre-Walker.

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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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