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.

Evolution of cooperation and conflict in experimental bacterial populations

Abstract

A fundamental problem in biology is the evolutionary transition from single cells to multicellular life forms1,2,3. During this transition the unit of selection shifts from individual cells to groups of cooperating cells1,3,4. Although there is much theory5,6,7,8,9,10,11,12,13,14,15, there are few empirical studies16. Here we describe an evolutionary transition that occurs in experimental populations of Pseudomonas fluorescens propagated in a spatially heterogeneous environment17. Cooperating groups are formed by over-production of an adhesive polymer18, which causes the interests of individuals to align with those of the group. The costs and benefits of cooperation, plus evolutionary susceptibility to defecting genotypes, were analysed to determine conformation to theory1,3,12. Cooperation was costly to individuals, but beneficial to the group. Defecting genotypes evolved in populations founded by the cooperating type and were fitter in the presence of this type than in its absence. In the short term, defectors sabotaged the viability of the group; but these findings nevertheless show that transitions to higher orders of complexity are readily achievable, provide insights into the selective conditions, and facilitate experimental analysis of the evolution of individuality.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Growth form and niche preference of studied bacteria.
Figure 2: Evolutionary emergence of defecting genotypes from WS during the course of selection in spatially heterogeneous microcosms.
Figure 3: Population dynamics of WS and defector genotypes in the presence and absence of competition.

References

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

    Google Scholar 

  2. Bonner, J. T. First Signals: The Evolution of Multicellular Development, (Princeton Univ. Press, Princeton, 2000)

    Google Scholar 

  3. Buss, L. W. The Evolution of Individuality (Princeton Univ. Press, Princeton, 1987)

    Google Scholar 

  4. Maynard Smith, J. in Evolutionary Progress (ed. Nitecki, M. H.) 219–230 (Univ. Chicago Press, Chicago, 1988)

    Google Scholar 

  5. Hamilton, W. D. The genetical evolution of social behaviour. J. Theor. Biol. 7, 1–52 (1964)

    CAS  Article  Google Scholar 

  6. Williams, G. C. Adaptation and Natural Selection (Princeton Univ. Press, Princeton, 1966)

    Google Scholar 

  7. Wilson, D. S. A theory of group selection. Proc. Natl Acad. Sci. USA 72, 143–146 (1975)

    ADS  CAS  Article  Google Scholar 

  8. Dawkins, R. The Selfish Gene (Oxford Univ. Press, Oxford, 1976)

    Google Scholar 

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

    ADS  MathSciNet  CAS  Article  Google Scholar 

  10. Ferriere, R. & Michod, R. E. The evolution of cooperation in spatially heterogeneous populations. Am. Nat. 147, 692–717 (1996)

    Article  Google Scholar 

  11. Sober, E. & Wilson, D. S. Unto Others: The Evolution and Psychology of Unselfish Behaviour (Harvard Univ. Press, Cambridge, MA, 1998)

    Google Scholar 

  12. Michod, R. E. Darwinian Dynamics: Evolutionary Transitions in Fitness and Individuality (Princeton Univ. Press, Princeton, 1999)

    MATH  Google Scholar 

  13. Pfeiffer, T., Schuster, S. & Bonhoeffer, S. Cooperation and competition in the evolution of ATP-producing pathways. Science 292, 504–507 (2001)

    ADS  CAS  Article  Google Scholar 

  14. Smith, J. The social evolution of bacterial pathogenesis. Proc. R. Soc. Lond. B 268, 61–69 (2001)

    CAS  Article  Google Scholar 

  15. Pfeiffer, T. & Bonhoeffer, S. An evolutionary scenario for the transition to undifferentiated multicellularity. Proc. Natl Acad. Sci. USA 100, 1095–1098 (2003)

    ADS  CAS  Article  Google Scholar 

  16. Boraas, M. E., Seale, D. B. & Boxhorn, J. E. Phagotrophy by a flagellate selects for colonial prey: A possible origin of multicellularity. Evol. Ecol. 12, 153–164 (1998)

    Article  Google Scholar 

  17. Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998)

    ADS  CAS  Article  Google Scholar 

  18. Spiers, A. J., Kahn, S. G., Bohannon, J., Travisano, M. & Rainey, P. B. Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161, 33–46 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Wolpert, L. The evolution of development. Biol. J. Linn. Soc. 39, 109–124 (1990)

    Article  Google Scholar 

  20. Bell, G. in The Origin and Evolution of Sex (eds Halvorson, H. & Mornoy, A.) 221–256 (Alan R. Liss, New York, 1985)

    Google Scholar 

  21. Koufopanou, V. & Bell, G. Soma and germ - an experimental approach using Volvox. Proc. R. Soc. Lond. B 254, 107–113 (1993)

    ADS  Article  Google Scholar 

  22. Kerszberg, M. & Wolpert, L. The origin of metazoa and the egg: a role for cell death. J. Theor. Biol. 193, 535–537 (1998)

    CAS  Article  Google Scholar 

  23. Foster, K. R., Fortunato, A., Strassmann, J. E. & Queller, D. C. The costs and benefits of being a chimera. Proc. R. Soc. Lond. B 269, 2357–2362 (2002)

    Article  Google Scholar 

  24. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991)

    Article  Google Scholar 

  25. Buckling, A., Kassen, R., Bell, G. & Rainey, P. B. Disturbance and diversity in experimental microcosms. Nature 408, 961–964 (2000)

    ADS  CAS  Article  Google Scholar 

  26. Hardin, G. The tragedy of the commons. Science 162, 1243–1248 (1968)

    ADS  CAS  Article  Google Scholar 

  27. Kassen, R., Buckling, A., Bell, G. & Rainey, P. B. Diversity peaks at intermediate productivity in a laboratory microcosm. Nature 406, 508–512 (2000)

    ADS  CAS  Article  Google Scholar 

  28. Frank, S. A. Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377, 520–522 (1995)

    ADS  CAS  Article  Google Scholar 

  29. 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)

    ADS  CAS  Article  Google Scholar 

  30. Wolf, J. B. Genetic architecture and evolutionary constraint when the environment contains genes. Proc. Natl Acad. Sci. USA 100, 4655–4660 (2003)

    ADS  CAS  Article  Google Scholar 

  31. Velicer, G. J. & Yu, Y. N. Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425 75–78 (2003)

    ADS  CAS  Article  Google Scholar 

Download references

Acknowledgements

We are grateful to D. S. Wilson and A. Buckling whose comments improved the manuscript. A Biotechnology and Biological Sciences Research Council (UK) Research Fellowship to P.B.R. supported the work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul B. Rainey.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Rainey, P., Rainey, K. Evolution of cooperation and conflict in experimental bacterial populations. Nature 425, 72–74 (2003). https://doi.org/10.1038/nature01906

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01906

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.

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