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.

Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae

Nature volume 451, pages 1107–1110 (2008)Cite this article

Abstract

Cooperation is central to many major transitions in evolution, including the emergence of eukaryotic cells, multicellularity and eusociality1. Cooperation can be destroyed by the spread of cheater mutants that do not cooperate but gain the benefits of cooperation from others1,2. However, cooperation can be preserved if cheaters are facultative, cheating others but cooperating among themselves2. Several cheater mutants have been studied before, but no study has attempted a genome-scale investigation of the genetic opportunities for cheating. Here we describe such a screen in a social amoeba and show that cheating is multifaceted by revealing cheater mutations in well over 100 genes of diverse types. Many of these mutants cheat facultatively, producing more than their fair share of spores in chimaeras, but cooperating normally when clonal. These findings indicate that phenotypically stable cooperative systems may nevertheless harbour genetic conflicts. The opportunities for evolutionary moves and countermoves in such conflicts may select for the involvement of multiple pathways and numerous genes.

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: Cheater selection.
Figure 2: Cheating ability and sporulation of isolated mutant strains.
Figure 3: Spatial distribution of cheater and wild-type cells in developing chimaeras.

References

  1. Maynard Smith, J. & Szathmary, E. The Major Transition in Evolution (Freeman, Oxford, 1995)

    Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Greig, D. & Travisano, M. The Prisoner’s Dilemma and polymorphism in yeast SUC genes. Proc R. Soc. B 271 (Suppl. 3). S25–S26 (2004)

    Article  CAS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  5. 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  CAS  ADS  Google Scholar 

  6. 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  CAS  ADS  Google Scholar 

  7. 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  CAS  ADS  Google Scholar 

  8. Queller, D. C., Ponte, E., Bozzaro, S. & Strassmann, J. E. Single-gene Greenbeard effects in the social amoeba Dictyostelium discoideum. Science 299, 105–106 (2003)

    Article  CAS  ADS  Google Scholar 

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

    Article  CAS  ADS  Google Scholar 

  10. Velicer, G. J., Kroos, L. & Lenski, R. E. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12376–12380 (1998)

    Article  CAS  ADS  Google Scholar 

  11. Velicer, G. J., Kroos, L. & Lenski, R. E. Developmental cheating in the social bacterium Myxococcus xanthus. Nature 404, 598–601 (2000)

    Article  CAS  ADS  Google Scholar 

  12. Velicer, G. J. et al. Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc. Natl Acad. Sci. USA 103, 8107–8112 (2006)

    Article  CAS  ADS  Google Scholar 

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

    Book  Google Scholar 

  14. Buss, L. W. Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl Acad. Sci. USA 79, 5337–5341 (1982)

    Article  CAS  ADS  Google Scholar 

  15. Filosa, M. F. Heterocytosis in cellular slime molds. Am. Nat. 96, 79–91 (1962)

    Article  Google Scholar 

  16. Fiegna, F. & Velicer, G. J. Exploitative and hierarchical antagonism in a cooperative bacterium. PLoS Biol. 3, e370 (2005)

    Article  Google Scholar 

  17. Chen, G., Shaulsky, G. & Kuspa, A. Tissue-specific G1-phase cell-cycle arrest prior to terminal differentiation in Dictyostelium. Development 131, 2619–2630 (2004)

    Article  CAS  Google Scholar 

  18. Shaulsky, G. & Loomis, W. F. Mitochondrial DNA replication but no nuclear DNA replication during development of Dictyostelium. Proc. Natl Acad. Sci. USA 92, 5660–5663 (1995)

    Article  CAS  ADS  Google Scholar 

  19. Sternfeld, J. & David, C. N. Fate and regulation of anterior-like cells in Dictyostelium slugs. Dev. Biol. 93, 111–118 (1982)

    Article  CAS  Google Scholar 

  20. Jermyn, K. A., Duffy, K. T. & Williams, J. G. A new anatomy of the prestalk zone in Dictyostelium. Nature 340, 144–146 (1989)

    Article  CAS  ADS  Google Scholar 

  21. Nielsen, R. Molecular signatures of natural selection. Annu. Rev. Genet. 39, 197–218 (2005)

    Article  CAS  Google Scholar 

  22. 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 

  23. Thompson, C. R., Fu, Q., Buhay, C., Kay, R. R. & Shaulsky, G. A bZIP/bRLZ transcription factor required for DIF signaling in Dictyostelium. Development 131, 513–523 (2004)

    Article  CAS  Google Scholar 

  24. Sussman, M. Cultivation and synchronous morphogenesis of Dictyostelium under controlled experimental conditions. Methods Cell Biol. 28, 9–29 (1987)

    Article  CAS  Google Scholar 

  25. 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  CAS  ADS  Google Scholar 

  26. 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  CAS  ADS  Google Scholar 

  27. Eichinger, L. et al. The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43–57 (2005)

    Article  CAS  ADS  Google Scholar 

  28. Kibler, K. et al. A novel developmental mechanism in Dictyostelium revealed in a screen for communication mutants. Dev. Biol. 259, 193–208 (2003)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank past and present members of our groups, especially A. Khare, E. Roberge, K. Foster and N. Mehdiabadi, for discussions and for technical assistance; R. H. Kessin for the fbxA- strain and for discussions; and W. F. Loomis for encouragement and advice. This work was supported by a grant from the National Science Foundation; L.A.S. was supported by a Wray–Todd Fellowship. C.R.L.T. was supported by the Wellcome Trust International Prize Traveling Research Fellowship.

Author Contributions L.A.S., C.R.L.T., E.V., J.S. and C.D. conducted the experimental work. A.P. and R.S. performed computational analyses. A.K., C.R.L.T., D.C.Q., G.S. and J.E.S. conceived of the study and wrote the paper. All authors discussed the results and commented on the manuscript.

Author information

Author notes

  1. Christopher R. L. Thompson

    Present address: Present address: Faculty of Life Sciences, Michael Smith Building, University of Manchester, Manchester M13 9PT, UK.,

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas 77005, USA,

    Lorenzo A. Santorelli, Adam Kuspa, Joan E. Strassmann, David C. Queller & Gad Shaulsky

  2. Department of Molecular and Human Genetics,,

    Christopher R. L. Thompson, Elizabeth Villegas, Jessica Svetz, Anup Parikh, Adam Kuspa & Gad Shaulsky

  3. Department of Biochemistry and Molecular Biology,,

    Christopher Dinh, Richard Sucgang & Adam Kuspa

  4. Graduate Program in Structural Computational Biology and Molecular Biophysics, Baylor College of Medicine, Houston, Texas 77030, USA,

    Anup Parikh & Gad Shaulsky

Authors
  1. Lorenzo A. Santorelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christopher R. L. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elizabeth Villegas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jessica Svetz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christopher Dinh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anup Parikh
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Richard Sucgang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Adam Kuspa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Joan E. Strassmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. David C. Queller
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Gad Shaulsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gad Shaulsky.

Supplementary information

Supplementary Information

The file contains Supplementary Notes; Supplementary Figures 1-5 with Legends; and Supplementary Tables 1-3. (PDF 1005 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Santorelli, L., Thompson, C., Villegas, E. et al. Facultative cheater mutants reveal the genetic complexity of cooperation in social amoebae. Nature 451, 1107–1110 (2008). https://doi.org/10.1038/nature06558

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06558

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