Snowdrift game dynamics and facultative cheating in yeast


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.

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Figure 1: Competition between the wild-type cooperator and mutant cheater strains.
Figure 2: Game theory models of cooperation in sucrose metabolism.
Figure 3: Varying the glucose concentration can transform the outcome of competition.


  1. 1

    Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981)

    ADS  MathSciNet  CAS  Article  Google Scholar 

  2. 2

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

    ADS  CAS  Article  Google Scholar 

  3. 3

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

    Google Scholar 

  4. 4

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

    CAS  Article  Google Scholar 

  5. 5

    West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4, 597–607 (2006)

    CAS  Article  Google Scholar 

  6. 6

    Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Shou, W., Ram, S. & Vilar, J. M. G. Synthetic cooperation in engineered yeast populations. Proc. Natl Acad. Sci. USA 104, 1877–1882 (2007)

    ADS  CAS  Article  Google Scholar 

  8. 8

    Diggle, S. P., Griffin, A. S., Campbell, G. S. & West, S. A. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411–414 (2007)

    ADS  CAS  Article  Google Scholar 

  9. 9

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

    ADS  CAS  Article  Google Scholar 

  10. 10

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

    CAS  Article  Google Scholar 

  11. 11

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

    ADS  CAS  Article  Google Scholar 

  12. 12

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

    ADS  CAS  Article  Google Scholar 

  13. 13

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

    CAS  Article  Google Scholar 

  14. 14

    Dickinson, J. R. & Schweizer, M. The Metabolism and Molecular Physiology of Saccharomyces cerevisiae 54–55 (CRC, 2004)

    Google Scholar 

  15. 15

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

    Article  Google Scholar 

  16. 16

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

    CAS  Article  Google Scholar 

  17. 17

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

    Article  Google Scholar 

  18. 18

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

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 19

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

    CAS  Article  Google Scholar 

  20. 20

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

    Google Scholar 

  21. 21

    Ozcan, S., Vallier, L. G., Flick, J. S., Carlson, M. & Johnston, M. Expression of the SUC2 gene of Saccharomyces cerevisiae is induced by low levels of glucose. Yeast 13, 127–137 (1997)

    CAS  Article  Google Scholar 

  22. 22

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

    ADS  CAS  Article  Google Scholar 

  23. 23

    Nowak, M. A. & May, R. M. Evolutionary games and spatial chaos. Nature 359, 826–829 (1992)

    ADS  Article  Google Scholar 

  24. 24

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

    Article  Google Scholar 

  25. 25

    Naumov, G. I., Naumova, E. S., Sancho, E. D. & Korhola, M. P. Polymeric SUC genes in natural populations of Saccharomyces cerevisiae . FEMS Microbiol. Lett. 135, 31–35 (1996)

    CAS  Article  Google Scholar 

  26. 26

    Kerr, B., Riley, M. A., Feldman, M. W. & Bohannan, B. J. M. Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418, 171–174 (2002)

    ADS  CAS  Article  Google Scholar 

  27. 27

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

    ADS  CAS  Article  Google Scholar 

  28. 28

    Keymer, J. E., Galajda, P., Muldoon, C., Park, S. & Austin, R. H. Bacterial metapopulations in nanofabricated landscapes. Proc. Natl Acad. Sci. USA 103, 17290–17295 (2006)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Nadell, C. D., Xavier, J. B. & Foster, K. R. The sociobiology of biofilms. FEMS Microbiol. Rev. 33, 206–224 (2009)

    CAS  Article  Google Scholar 

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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.

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Correspondence to Alexander van Oudenaarden.

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Gore, J., Youk, H. & van Oudenaarden, A. Snowdrift game dynamics and facultative cheating in yeast. Nature 459, 253–256 (2009).

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