Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Experimental evolution reveals natural selection on standing genetic variation

Abstract

Evolution depends on genetic variation generated by mutation or recombination from standing genetic variation. In sexual organisms, little is known about the molecular population genetics of adaptation and reverse evolution1,2,3,4,5,6,7,8,9,10,11. We carry out 50 generations of experimental reverse evolution in populations of Drosophila melanogaster, previously differentiated by forward evolution, and follow changes in the frequency of SNPs in both arms of the third chromosome. We characterize the effects of sampling finite population sizes and natural selection at the genotype level. We demonstrate that selection has occurred at several loci and further that there is no general loss or gain of allele diversity. We also observe that despite the complete convergence to ancestral levels of adaptation, allele frequencies only show partial return.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Experimental evolution design.
Figure 2: Population dynamics of SNPs.
Figure 3: Loci undergoing independent evolution.
Figure 4: Effects of sampling finite populations.
Figure 5: Reverse evolution at the genotype level.

Similar content being viewed by others

References

  1. Cohan, F.M. Can uniform selection retard random genetic divergence between isolated conspecific populations. Evolution Int. J. Org. Evolution 38, 495–504 (1984).

    Article  Google Scholar 

  2. Travisano, M., Mongold, J.A., Bennett, A.F. & Lenski, R.E. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267, 87–90 (1995).

    Article  CAS  PubMed  Google Scholar 

  3. Crill, W.D., Wichman, H.A. & Bull, J.J. Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154, 27–37 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Teotónio, H. & Rose, M.R. Variation in the reversibility of evolution. Nature 408, 463–466 (2000).

    Article  PubMed  Google Scholar 

  5. Bull, J.J. & Charnov, E.L. On irreversible evolution. Evolution Int. J. Org. Evolution 39, 1149–1155 (1985).

    Article  CAS  Google Scholar 

  6. Teotónio, H. & Rose, M.R. Perspective: reverse evolution. Evolution Int. J. Org. Evolution 55, 653–660 (2001).

    Article  Google Scholar 

  7. Teotónio, H., Matos, M. & Rose, M.R. Reverse evolution of fitness in Drosophila melanogaster. J. Evol. Biol. 15, 608–617 (2002).

    Article  Google Scholar 

  8. Grant, P.R. & Grant, B.R. Unpredictable evolution in a 30-year study of Darwin's finches. Science 296, 707–711 (2002).

    Article  CAS  PubMed  Google Scholar 

  9. Whiting, M.F., Bradler, S. & Maxwell, T. Loss and recovery of wings in stick insects. Nature 421, 264–267 (2003).

    Article  CAS  PubMed  Google Scholar 

  10. Whitlock, M.C., Phillips, P.C. & Fowler, K. Persistence of changes in the genetic covariance matrix after a bottleneck. Evolution Int. J. Org. Evolution 56, 1968–1975 (2002).

    Article  Google Scholar 

  11. Porter, M.L. & Crandall, K.A. Lost along the way: the significance of evolution in reverse. Trends Ecol. Evol. 18, 541–547 (2003).

    Article  Google Scholar 

  12. Colosimo, P.F. et al. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307, 1928–1933 (2005).

    Article  CAS  PubMed  Google Scholar 

  13. Teotónio, H., Matos, M. & Rose, M.R. Quantitative genetics of functional characters in Drosophila melanogaster populations subjected to laboratory selection. J. Genet. 83, 265–277 (2004).

    Article  PubMed  Google Scholar 

  14. Hudson, R.R., Sáez, A.G. & Ayala, F.J. DNA variation at the Sod locus of Drosophila meanogaster: an unfolding story of natural selection. Proc. Natl. Acad. Sci. USA 94, 7725–7729 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Deckert-Cruz, D.J., Tyler, R.H., Landmesser, J.E. & Rose, M.R. Allozymic differentiation in response to laboratory demographic selection of Drosophila melanogaster. Evolution Int. J. Org. Evolution 51, 865–872 (1997).

    Article  Google Scholar 

  16. Verrelli, B.C. & Eanes, W.F. Clinal variation for amino acid polymorphisms at the Pgm locus in Drosophila melanogaster. Genetics 157, 1649–1663 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Balakirev, E.S., Anisimova, M. & Ayala, F.J. Positive and negative selection in the β-Esterase gene cluster of the Drosophila melanogaster subgroup. J. Mol. Evol. 62, 496–510 (2006).

    Article  CAS  PubMed  Google Scholar 

  18. Smith, J.M. & Haigh, J. The hitch-hiking effect of a favourable gene. Genet. Res. 23, 23–35 (1974).

    Article  CAS  PubMed  Google Scholar 

  19. Hartl, D.L. & Clark, A.G. Principles of Population Genetics (Sinauer, Sunderland, Massachusetts, 1989).

    Google Scholar 

  20. Macdonald, S.J., Pasten, T. & Long, A.D. The effect of polymorphisms in the Enhancer of split gene complex on bristle number variation in a large wild-caught cohort of Drosophila melanogaster. Genetics 171, 1741–1756 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Scheet, P. & Stephens, M. Fast and flexible model for LD. Am. J. Hum. Genet. 78, 629–644 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. McVean, G., Awadalla, P. & Fearnhead, P. A coalescent-based method for detecting and estimating recombination rates from gene sequences. Genetics 160, 1231–1241 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Nei, M. & Tajima, F. Genetic drift and the estimation of effective population size. Genetics 98, 625–640 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Goldringer, I. & Bataillon, T. On the distribution of temporal variations in allele frequency: consequences for the estimation of effective population size and the detection of loci undergoing selection. Genetics 168, 563–568 (2004).

    Article  PubMed  PubMed Central  Google Scholar 

  25. Nei, M. Definition and estimation of fixation indices. Evolution Int. J. Org. Evolution 40, 643–645 (1986).

    Article  Google Scholar 

  26. Churchill, G.A. & Doerge, R.W. Empirical threshold values for quantitative trait mapping. Genetics 138, 963–971 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Hermisson, J. & Pennings, P.S. Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169, 2335–2352 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2006).

  29. Haag-Liautard, C. et al. Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila. Nature 445, 82–85 (2007).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank T. Aires, D. Brites, J. Costa and I. Marques for support with SNP discovery and genotyping, and G. McVean for support with LDhat. We thank R. Azevedo, S. Carvalho, A. Coutinho, S. Estes, L. Mueller, P. Phillips, S. Proulx, M. Che Soares and É. Sucena for comments on the project and manuscript. Financial support was provided by The National Science Foundation to A.D.L. (DEB-0614429), and Fundação para a Ciência e a Tecnologia (FCT/FEDER POCTI/BSE/48228/2002) and Fundação Calouste Gulbenkian to H.T.

Author information

Authors and Affiliations

Authors

Contributions

H.T., I.M.C. and M.B. performed the experiments. H.T., I.M.C. and A.D.L. analysed the data. H.T., M.R.R. and A.D.L. conceived the project and wrote the manuscript.

Corresponding author

Correspondence to Henrique Teotónio.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 and Supplementary Tables 1–6 (PDF 513 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Teotónio, H., Chelo, I., Bradić, M. et al. Experimental evolution reveals natural selection on standing genetic variation. Nat Genet 41, 251–257 (2009). https://doi.org/10.1038/ng.289

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng.289

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing