Letter | Published:

Snowdrift game dynamics and facultative cheating in yeast

Nature volume 459, pages 253256 (14 May 2009) | Download Citation

Subjects

Abstract

The origin of cooperation is a central challenge to our understanding of evolution1,2,3. The fact that microbial interactions can be manipulated in ways that animal interactions cannot has led to a growing interest in microbial models of cooperation4,5,6,7,8,9,10 and competition11,12. For the budding yeast Saccharomyces cerevisiae to grow on sucrose, the disaccharide must first be hydrolysed by the enzyme invertase13,14. This hydrolysis reaction is performed outside the cytoplasm in the periplasmic space between the plasma membrane and the cell wall. Here we demonstrate that the vast majority (99 per cent) of the monosaccharides created by sucrose hydrolysis diffuse away before they can be imported into the cell, serving to make invertase production and secretion a cooperative behaviour15,16. A mutant cheater strain that does not produce invertase is able to take advantage of and invade a population of wild-type cooperator cells. However, over a wide range of conditions, the wild-type cooperator can also invade a population of cheater cells. Therefore, we observe steady-state coexistence between the two strains in well-mixed culture resulting from the fact that rare strategies outperform common strategies—the defining features of what game theorists call the snowdrift game17. A model of the cooperative interaction incorporating nonlinear benefits explains the origin of this coexistence. We are able to alter the outcome of the competition by varying either the cost of cooperation or the glucose concentration in the media. Finally, we note that glucose repression of invertase expression in wild-type cells produces a strategy that is optimal for the snowdrift game—wild-type cells cooperate only when competing against cheater cells.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    & The evolution of cooperation. Science 211, 1390–1396 (1981)

  2. 2.

    Five rules for the evolution of cooperation. Science 314, 1560–1563 (2006)

  3. 3.

    Evolution and the Theory of Games 167–173 (Cambridge Univ. Press, 1982)

  4. 4.

    Social strife in the microbial world. Trends Microbiol. 11, 330–337 (2003)

  5. 5.

    , , & Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4, 597–607 (2006)

  6. 6.

    , & Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004)

  7. 7.

    , & Synthetic cooperation in engineered yeast populations. Proc. Natl Acad. Sci. USA 104, 1877–1882 (2007)

  8. 8.

    , , & Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411–414 (2007)

  9. 9.

    & Evolution of cooperation and conflict in experimental bacterial populations. Nature 425, 72–74 (2003)

  10. 10.

    et al. FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell 135, 726–737 (2008)

  11. 11.

    & Resource competition and social conflict in experimental populations of yeast. Nature 441, 498–501 (2006)

  12. 12.

    & Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc. Natl Acad. Sci. USA 78, 6324–6328 (1981)

  13. 13.

    & 2 differentially regulated messenger-RNAs with different 5′ ends encode secreted and intracellular forms of yeast invertase. Cell 28, 145–154 (1982)

  14. 14.

    & The Metabolism and Molecular Physiology of Saccharomyces cerevisiae 54–55 (CRC, 2004)

  15. 15.

    & The Prisoner’s Dilemma and polymorphism in yeast SUC genes. Proc. R. Soc. Lond. B 271 (suppl.). 25–26 (2004)

  16. 16.

    & Stable public goods cooperation and dynamic social interactions in yeast. J. Evol. Biol. 21, 1836–1843 (2008)

  17. 17.

    & Models of cooperation based on the Prisoner’s Dilemma and the Snowdrift game. Ecol. Lett. 8, 748–766 (2005)

  18. 18.

    Yeast carbon catabolite repression. Microbiol. Mol. Biol. Rev. 62, 334–361 (1998)

  19. 19.

    Co-operation and defection: playing the field and the ESS. J. Theor. Biol. 151, 145–154 (1991)

  20. 20.

    The Stag Hunt and Evolution of Social Structure (Cambridge Univ. Press, 2004)

  21. 21.

    , , , & Expression of the SUC2 gene of Saccharomyces cerevisiae is induced by low levels of glucose. Yeast 13, 127–137 (1997)

  22. 22.

    et al. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107–1110 (2008)

  23. 23.

    & Evolutionary games and spatial chaos. Nature 359, 826–829 (1992)

  24. 24.

    & Competitive fates of bacterial social parasites: persistence and self-induced extinction of Myxococcus xanthus cheaters. Proc. R. Soc. Lond. B 270, 1527–1534 (2003)

  25. 25.

    , , & Polymeric SUC genes in natural populations of Saccharomyces cerevisiae. FEMS Microbiol. Lett. 135, 31–35 (1996)

  26. 26.

    , , & Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418, 171–174 (2002)

  27. 27.

    & Spatial structure often inhibits the evolution of cooperation in the snowdrift game. Nature 428, 643–646 (2004)

  28. 28.

    , , , & Bacterial metapopulations in nanofabricated landscapes. Proc. Natl Acad. Sci. USA 103, 17290–17295 (2006)

  29. 29.

    , & The sociobiology of biofilms. FEMS Microbiol. Rev. 33, 206–224 (2009)

Download references

Acknowledgements

The authors would like to thank D. Kim, A. Raj, K. Gora, D. Muzzey and B. Pando for discussions and/or experimental help. This work was supported by grants from the US National Institutes of Health (NIH) and National Science Foundation to A.v.O. J.G. is supported through a Pappalardo Postdoctoral Fellowship and an NIH K99 Pathways to Independence Award. H.Y. was supported by a Lester Wolfe Fellowship.

Author information

Affiliations

  1. Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA

    • Jeff Gore
    • , Hyun Youk
    •  & Alexander van Oudenaarden

Authors

  1. Search for Jeff Gore in:

  2. Search for Hyun Youk in:

  3. Search for Alexander van Oudenaarden in:

Corresponding author

Correspondence to Alexander van Oudenaarden.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Figure 1-12 with Legends, Supplementary Table 1 and Supplementary References

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature07921

Further reading Further reading

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.