Skip to main content

Thank you for visiting 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.

Cheater-resistance is not futile


Cooperative social systems are susceptible to cheating by individuals that reap the benefits of cooperation without incurring the costs1. There are various theoretical mechanisms for the repression of cheating2 and many have been tested experimentally. One possibility that has not been tested rigorously is the evolution of mutations that confer resistance to cheating. Here we show that the presence of a cheater in a population of randomly mutated social amoebae can select for cheater-resistance. Furthermore, we show that this cheater-resistance can be a noble strategy because the resister strain does not necessarily exploit other strains. Thus, the evolution of resisters may be instrumental in preserving cooperative behaviour in the face of cheating.

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


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

Figure 1: The presence of a cheater selects for cheater-resistance.
Figure 2: rccA is a noble, specific cheater-resister.
Figure 3: Cheater-resistance is a general phenomenon.


  1. Maynard Smith, J. & Szathmáry, E. The Major Transitions in Evolution (Oxford Univ. Press, 1997)

    Google Scholar 

  2. Travisano, M. & Velicer, G. J. Strategies of microbial cheater control. Trends Microbiol. 12, 72–78 (2004)

    Article  CAS  Google Scholar 

  3. Kessin, R. H. Dictyostelium: Evolution, Cell Biology, and the Development of Multicellularity (Cambridge Univ. Press, 2001)

    Book  Google Scholar 

  4. Strassmann, J. E., Zhu, Y. & Queller, D. C. Altruism and social cheating in the social amoeba Dictyostelium discoideum . Nature 408, 965–967 (2000)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  6. Ennis, H. L., Dao, D. N., Pukatzki, S. U. & Kessin, R. H. Dictyostelium amoebae lacking an F-box protein form spores rather than stalk in chimeras with wild type. Proc. Natl Acad. Sci. USA 97, 3292–3297 (2000)

    Article  ADS  CAS  Google Scholar 

  7. Foster, K. R., Shaulsky, G., Strassmann, J. E., Queller, D. C. & Thompson, C. R. L. Pleiotropy as a mechanism to stabilize cooperation. Nature 431, 693–696 (2004)

    Article  ADS  CAS  Google Scholar 

  8. Gilbert, O. M., Foster, K. R., Mehdiabadi, N. J., Strassmann, J. E. & Queller, D. C. High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants. Proc. Natl Acad. Sci. USA 104, 8913–8917 (2007)

    Article  ADS  CAS  Google Scholar 

  9. Mehdiabadi, N. J. et al. Social evolution: kin preference in a social microbe. Nature 442, 881–882 (2006)

    Article  ADS  CAS  Google Scholar 

  10. Ostrowski, E. A., Katoh, M., Shaulsky, G., Queller, D. C. & Strassmann, J. E. Kin discrimination increases with genetic distance in a social amoeba. PLoS Biol. 6, e287 (2008)

    Article  Google Scholar 

  11. Fiegna, F., Yu, Y. T. N., Kadam, S. V. & Velicer, G. J. Evolution of an obligate social cheater to a superior cooperator. Nature 441, 310–314 (2006)

    Article  ADS  CAS  Google Scholar 

  12. Marques, J. T. & Carthew, R. W. A call to arms: coevolution of animal viruses and host innate immune responses. Trends Genet. 23, 359–364 (2007)

    Article  CAS  Google Scholar 

  13. Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581–608 (2006)

    Article  CAS  Google Scholar 

  14. Clutton-Brock, T. H. & Parker, G. A. Punishment in animal societies. Nature 373, 209–216 (1995)

    Article  ADS  CAS  Google Scholar 

  15. Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. The evolution of cooperation. Q. Rev. Biol. 79, 135–160 (2004)

    Article  Google Scholar 

  16. Vulic, M. & Kolter, R. Evolutionary cheating in Escherichia coli stationary phase cultures. Genetics 158, 519–526 (2001)

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  19. Knecht, D. A., Cohen, S. M., Loomis, W. F. & Lodish, H. F. Developmental regulation of Dictyostelium discoideum actin gene fusions carried on low-copy and high-copy transformation vectors. Mol. Cell. Biol. 6, 3973–3983 (1986)

    Article  CAS  Google Scholar 

  20. Faix, J., Kreppel, L., Shaulsky, G., Schleicher, M. & Kimmel, A. R. A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Res. 32, e143 (2004)

    Article  Google Scholar 

  21. Shaulsky, G., Escalante, R. & Loomis, W. F. Developmental signal transduction pathways uncovered by genetic suppressors. Proc. Natl Acad. Sci. USA 93, 15260–15265 (1996)

    Article  ADS  CAS  Google Scholar 

  22. Kuspa, A. & Loomis, W. F. Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc. Natl Acad. Sci. USA 89, 8803–8807 (1992)

    Article  ADS  CAS  Google Scholar 

  23. Katoh, M. et al. Developmentally regulated DNA methylation in Dictyostelium discoideum . Eukaryot. Cell 5, 18–25 (2006)

    Article  CAS  Google Scholar 

  24. Vollrath, D., Davis, R. W., Connelly, C. & Hieter, P. Physical mapping of large DNA by chromosome fragmentation. Proc. Natl Acad. Sci. USA 85, 6027–6031 (1988)

    Article  ADS  CAS  Google Scholar 

  25. Feinberg, A. P. & Vogelstein, B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6–13 (1983)

    Article  CAS  Google Scholar 

  26. Huang, E. et al. bZIP transcription factor interactions regulate DIF responses in Dictyostelium . Development 133, 449–458 (2006)

    Article  CAS  Google Scholar 

Download references


This work was supported by a grant from the National Science Foundation. A. Khare was supported by a pre-doctoral fellowship from the Cullen Foundation.

Author Contributions A. Khare conducted the experimental work and wrote the paper, L.A.S. isolated the original LAS5 and LAS1 cheater strains. All of the authors conceived the study, discussed the results and commented on the manuscript.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Gad Shaulsky.

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Khare, A., Santorelli, L., Strassmann, J. et al. Cheater-resistance is not futile. Nature 461, 980–982 (2009).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


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.


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