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.

Incipient speciation by divergent adaptation and antagonistic epistasis in yeast

Nature volume 447, pages 585–588 (2007)Cite this article

Abstract

Establishing the conditions that promote the evolution of reproductive isolation and speciation has long been a goal in evolutionary biology1,2,3. In ecological speciation, reproductive isolation between populations evolves as a by-product of divergent selection and the resulting environment-specific adaptations4,5,6. The leading genetic model of reproductive isolation predicts that hybrid inferiority is caused by antagonistic epistasis between incompatible alleles at interacting loci1,7. The fundamental link between divergent adaptation and reproductive isolation through genetic incompatibilities has been predicted1,4,5, but has not been directly demonstrated experimentally. Here we empirically tested key predictions of speciation theory by evolving the initial stages of speciation in experimental populations of the yeast Saccharomyces cerevisiae. After replicate populations adapted to two divergent environments, we consistently observed the evolution of two forms of postzygotic isolation in hybrids: reduced rate of mitotic reproduction and reduced efficiency of meiotic reproduction. This divergent selection resulted in greater reproductive isolation than parallel selection, as predicted by the ecological speciation theory. Our experimental system allowed controlled comparison of the relative importance of ecological and genetic isolation, and we demonstrated that hybrid inferiority can be ecological and/or genetic in basis. Overall, our results show that adaptation to divergent environments promotes the evolution of reproductive isolation through antagonistic epistasis, providing evidence of a plausible common avenue to speciation and adaptive radiation in nature.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Figure 1: Comparisons of mitotic fitness.
Figure 2: General patterns of mitotic fitness across population classes.
Figure 3: Comparisons of meiotic efficiency.

References

  1. Dobzhansky, T. Genetics and the Origin of Species (Columbia Univ. Press, New York, 1937)

    Google Scholar 

  2. Coyne, J. A. Genetics and speciation. Nature 355, 511–515 (1992)

    Article  ADS  CAS  Google Scholar 

  3. Coyne, J. A. & Orr, H. A. Speciation (Sinauer, Sunderland, 2004)

    Google Scholar 

  4. Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, 2000)

    Google Scholar 

  5. Schluter, D. Ecology and the origin of species. Trends Ecol. Evol. 16, 372–380 (2001)

    Article  CAS  Google Scholar 

  6. Rundle, H. D. & Nosil, P. Ecological speciation. Ecol. Lett. 8, 336–352 (2005)

    Article  Google Scholar 

  7. Muller, H. J. Isolating mechanisms, evolution, and temperature. Biol. Symp. 6, 71–125 (1942)

    Google Scholar 

  8. McKinnon, J. S. et al. Evidence for ecology’s role in speciation. Nature 429, 294–298 (2004)

    Article  ADS  CAS  Google Scholar 

  9. Funk, D. J., Nosil, P. & Etges, W. J. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc. Natl Acad. Sci. USA 103, 3209–3213 (2006)

    Article  ADS  CAS  Google Scholar 

  10. Orr, H. A. & Turelli, M. The evolution of postzygotic isolation: accumulating Dobzhansky–Muller incompatibilities. Evolution 55, 1085–1094 (2001)

    Article  CAS  Google Scholar 

  11. Presgraves, D. C., Balagopalan, L., Abmayr, S. M. & Orr, H. A. Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423, 715–719 (2003)

    Article  ADS  CAS  Google Scholar 

  12. Rundle, H. D. & Whitlock, M. C. A genetic interpretation of ecologically dependent isolation. Evolution 55, 198–201 (2001)

    Article  CAS  Google Scholar 

  13. Demuth, J. P. & Wade, M. J. On the theoretical and empirical framework for studying genetic interactions within and among species. Am. Nat. 165, 524–536 (2005)

    Article  Google Scholar 

  14. Anderson, J. B., Ricker, N. & Sirjusingh, C. Antagonism between two mechanisms of antifungal drug resistance. Eukaryot. Cell 5, 1243–1251 (2006)

    Article  CAS  Google Scholar 

  15. Rieseberg, L. H. Chromosomal rearrangements and speciation. Trends Ecol. Evol. 16, 351–358 (2001)

    Article  Google Scholar 

  16. Delneri, D. et al. Engineering evolution to study speciation in yeasts. Nature 422, 68–72 (2003)

    Article  ADS  CAS  Google Scholar 

  17. Fischer, G., James, S. A., Roberts, I. N., Oliver, S. G. & Louis, E. J. Chromosomal evolution in Saccharomyces. Nature 405, 451–454 (2000)

    Article  ADS  CAS  Google Scholar 

  18. Hunter, N., Chambers, S. R., Louis, E. J. & Borts, R. H. The mismatch repair system contributes to meiotic sterility in an interspecific yeast hybrid. EMBO J. 15, 1726–1733 (1996)

    Article  CAS  Google Scholar 

  19. Greig, D., Travisano, M., Louis, E. J. & Borts, R. H. A role for the mismatch repair system during incipient speciation in Saccharomyces. J. Evol. Biol. 16, 429–437 (2003)

    Article  CAS  Google Scholar 

  20. Chu, S. et al. The transcriptional program of sporulation in budding yeast. Science 282, 699–705 (1998)

    Article  ADS  CAS  Google Scholar 

  21. Greig, D. A screen for recessive speciation genes expressed in the gametes of F1 hybrid yeast. PLoS Genet. 3, e21 (2007)

    Article  Google Scholar 

  22. Greig, D., Borts, R. H., Louis, E. J. & Travisano, M. Epistasis and hybrid sterility in Saccharomyces. Proc. R. Soc. Lond. B 269, 1167–1171 (2002)

    Article  Google Scholar 

  23. Rice, W. R. & Hostert, E. E. Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47, 1637–1653 (1993)

    Article  Google Scholar 

  24. Mooers, A. Ø., Rundle, H. D. & Whitlock, M. C. The effects of selection and bottlenecks on male mating success in peripheral isolates. Am. Nat. 153, 437–444 (1999)

    Article  Google Scholar 

  25. Rundle, H. D. Divergent environments and population bottlenecks fail to generate premating isolation in Drosophila pseudoobscura. Evolution 57, 2557–2565 (2003)

    Article  Google Scholar 

  26. Rundle, H. D., Chenoweth, S. F., Doughty, P. & Blows, M. W. Divergent selection and the evolution of signal traits and mating preferences. PLoS Biol. 3, e368 (2005)

    Article  Google Scholar 

  27. Leu, J. Y. & Murray, A. W. Experimental evolution of mating discrimination in budding yeast. Curr. Biol. 16, 280–286 (2006)

    Article  CAS  Google Scholar 

  28. de Oliveira, A. K. & Cordeiro, A. R. Adaptation of Drosophila willistoni experimental populations to extreme pH medium II. Development of incipient reproductive isolation. Heredity 44, 123–130 (1980)

    Article  Google Scholar 

  29. Kohn, L. M. Mechanisms of fungal speciation. Annu. Rev. Phytopathol. 43, 279–308 (2005)

    Article  CAS  Google Scholar 

  30. Anderson, J. B. et al. Mode of selection and experimental evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics 163, 1287–1298 (2003)

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by Discovery grants to J.B.A. and L.M.K., and a Postdoctoral Fellowship to J.R.D., from the Natural Science and Engineering Research Council of Canada.

Author Contributions The research was conceived and planned by all authors. C.S. and J.R.D. performed the experiments, and J.R.D. analysed the data. J.R.D, J.B.A. and L.M.K. contributed to the writing of the manuscript, which was coordinated by J.R.D.

The full microarray data set has been deposited in the Gene Expression Omnibus (http://www.ncbi.nlm.nih.gov/geo/) under accession series GSE6870.

Author information

Authors and Affiliations

  1. Department of Ecology & Evolutionary Biology, University of Toronto, Mississauga, Ontario, L5L 1C6, Canada,

    Jeremy R. Dettman, Caroline Sirjusingh, Linda M. Kohn & James B. Anderson

Authors
  1. Jeremy R. Dettman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Caroline Sirjusingh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Linda M. Kohn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James B. Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jeremy R. Dettman.

Ethics declarations

Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file includes Supplementary Methods, Supplementary Material 1 (Evidence against alternative explanations for reduced meiotic efficiency of hybrids), Supplementary Material 2 (Genetic experiment to assess concomitant reductions in mitotic fitness and meiotic efficiency) Supplementary Material 3 (Microarray expression data), and Supplementary Material 4 (Validation of microarray expression data). (PDF 1199 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dettman, J., Sirjusingh, C., Kohn, L. et al. Incipient speciation by divergent adaptation and antagonistic epistasis in yeast. Nature 447, 585–588 (2007). https://doi.org/10.1038/nature05856

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature05856

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced 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