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Adaptive protein evolution in Drosophila

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 Ps > 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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Correspondence to Adam 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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