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.

  • Letter
  • Published:

Local migration promotes competitive restraint in a host–pathogen 'tragedy of the commons'


Fragmented populations possess an intriguing duplicity: even if subpopulations are reliably extinction-prone, asynchrony in local extinctions and recolonizations makes global persistence possible1,2,3,4,5,6,7,8. Migration is a double-edged sword in such cases: too little migration prevents recolonization of extinct patches, whereas too much synchronizes subpopulations, raising the likelihood of global extinction. Both edges of this proverbial sword have been explored by manipulating the rate of migration within experimental populations1,3,4,5,6,8. However, few experiments have examined how the evolutionary ecology of fragmented populations depends on the pattern of migration5. Here, we show that the migration pattern affects both coexistence and evolution within a community of bacterial hosts (Escherichia coli) and viral pathogens (T4 coliphage) distributed across a large network of subpopulations. In particular, different patterns of migration select for distinct pathogen strategies, which we term 'rapacious' and 'prudent'. These strategies define a 'tragedy of the commons'9: rapacious phage displace prudent variants for shared host resources, but prudent phage are more productive when alone. We find that prudent phage dominate when migration is spatially restricted, while rapacious phage evolve under unrestricted migration. Thus, migration pattern alone can determine whether a de novo tragedy of the commons is resolved in favour of restraint.

This is a preview of subscription content, access via your institution

Access options

Buy this article

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

Figure 1: Stochastic cellular automata predictions.
Figure 2: Ecological and evolutionary results for experimental metapopulations.
Figure 3: Evolutionary stochastic cellular automata.

Similar content being viewed by others


  1. Bonsall, M. B., French, D. R. & Hassell, M. P. Metapopulation structures affect persistence of predator–prey interactions. J. Anim. Ecol. 71, 1075–1084 (2002)

    Article  Google Scholar 

  2. Briggs, C. J. & Hoopes, M. F. Stabilizing effects in spatial parasitoid–host and predator–prey models: a review. Theor. Popul. Biol. 65, 299–315 (2004)

    Article  PubMed  Google Scholar 

  3. Ellner, S. P. et al. Habitat structure and population persistence in an experimental community. Nature 412, 538–543 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  4. Holyoak, M. & Lawler, S. P. Persistence of an extinction-prone predator–prey interaction through metapopulation dynamics. Ecology 77, 1867–1879 (1996)

    Article  Google Scholar 

  5. Holyoak, M. Habitat patch arrangement and metapopulation persistence of predators and prey. Am. Nat. 156, 378–389 (2000)

    Article  Google Scholar 

  6. Huffaker, C. B. Experimental studies on predation: dispersion factors and predator–prey oscillations. Hilgardia 27, 343–383 (1958)

    Article  Google Scholar 

  7. Johst, K. & Schops, K. Persistence and conservation of a consumer-resource metapopulation with local overexploitation of resources. Biol. Conserv. 109, 57–65 (2003)

    Article  Google Scholar 

  8. Thrall, P. H., Godfree, R. & Burdon, J. J. Influence of spatial structure on pathogen colonization and extinction: a test using an experimental metapopulation. Plant Pathol. 52, 350–361 (2003)

    Article  Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Holyoak, M., Leibold, M. A. & Holt, R. D. Metacommunities: Spatial Dynamics and Ecological Communities (Univ. Chicago Press, Chicago, 2005)

    Google Scholar 

  11. Antonovics, J. in Ecology, Genetics, and Evolution of Metapopulations (eds Hanski, I. & Gaggiotti, O. E.) 471–488 (Elsevier, Oxford, 2004)

    Book  Google Scholar 

  12. Grenfell, B., Bjørnstad, O. N. & Kappey, J. Travelling waves and spatial hierarchies in measles epidemics. Nature 414, 716–723 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  13. Keeling, M., Bjørnstad, O. N. & Grenfell, B. in Ecology, Genetics, and Evolution of Metapopulations (eds Hanski, I. & Gaggiotti, O. E.) 415–445 (Elsevier, Oxford, 2004)

    Book  Google Scholar 

  14. Abedon, S. T., Hyman, P. & Thomas, C. Experimental examination of bacteriophage latent-period evolution as a response to bacterial availability. Appl. Environ. Microbiol. 69, 7499–7506 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bohannan, B. J. M. & Lenski, R. E. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecol. Lett. 3, 362–377 (2000)

    Article  Google Scholar 

  16. Lenski, R. E. & Levin, B. R. Constraints on the coevolution of bacteria and virulent phage: a model, some experiments, and predictions for natural communities. Am. Nat. 125, 585–602 (1985)

    Article  Google Scholar 

  17. Paddison, P. et al. The roles of the bacteriophage T4 r genes in lysis inhibition and fine-structure genetics: A new perspective. Genetics 148, 1539–1550 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Keeling, M. Evolutionary trade-offs at two time-scales: competition versus persistence. Proc. R. Soc. Lond. B 267, 385–391 (2000)

    Article  CAS  Google Scholar 

  19. Kreft, J. U. Biofilms promote altruism. Microbiology 150, 2751–2760 (2004)

    Article  CAS  PubMed  Google Scholar 

  20. Bergstrom, C. T., McElhany, P. & Real, L. A. Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc. Natl Acad. Sci. USA 96, 5095–5100 (1999)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  21. Boots, M. & Sasaki, A. 'Small worlds' and the evolution of virulence: infection occurs locally and at a distance. Proc. R. Soc. Lond. B 266, 1933–1938 (1999)

    Article  CAS  Google Scholar 

  22. Bull, J. J., Molineux, I. J. & Rice, W. R. Selection of benevolence in a host–parasite system. Evolution 45, 875–882 (1991)

    Article  CAS  PubMed  Google Scholar 

  23. Cooper, V. S. et al. Timing of transmission and the evolution of virulence of an insect virus. Proc. R. Soc. Lond. B 269, 1161–1165 (2002)

    Article  Google Scholar 

  24. Ebert, D. Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084–1086 (1994)

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Galvani, A. P. Epidemiology meets evolutionary ecology. Trends Ecol. Evol. 18, 132–139 (2003)

    Article  Google Scholar 

  26. Herre, E. A. Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 1442–1445 (1993)

    Article  ADS  CAS  PubMed  Google Scholar 

  27. Lipsitch, M., Herre, E. A. & Nowak, M. A. Host population structure and the evolution of virulence: a 'law of diminishing returns'. Evolution 49, 743–748 (1995)

    PubMed  Google Scholar 

  28. Nowak, M. A. & May, R. M. Superinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B 255, 81–89 (1994)

    Article  ADS  CAS  Google Scholar 

  29. O'Keefe, K. J. & Antonovics, J. Playing by different rules: The evolution of virulence in sterilizing pathogens. Am. Nat. 159, 597–605 (2002)

    Article  PubMed  Google Scholar 

  30. Thrall, P. H. & Burdon, J. J. Evolution of virulence in a plant host–pathogen metapopulation. Science 299, 1735–1737 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

Download references


We thank Y. Dang for help in the laboratory and the BioTechnology Resource Center at the University of Minnesota for robot access. We thank S. Abedon, C. Bergstrom, J. Bull, J. Fletcher, K. Koelle, C. Lehman, B. Levin and D. Stephens for useful feedback on this project and manuscript. This work was partially supported by an NSF grant to C.N. and an NIH grant to A.M.D. Author Contributions B.K., A.M.D. and B.J.M.B. designed the experiments. B.K. and A.M.D. worked out the robotic protocols. B.K. programmed the robot, executed the experiments, and conducted the assays. B.K. and C.N. coded and analysed the empirically calibrated and evolutionary models. B.K., C.N. and A.M.D. conducted the statistical analysis. All authors contributed to the writing of the manuscript.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Benjamin Kerr.

Ethics declarations

Competing interests

Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Supplementary Methods

This file contains experimental and theoretical methods and results, giving a detailed description of the experimental methods used, presentation of experimental data, and its statistical analysis as well as the details concerning the construction and analysis of the theoretical models. (PDF 600 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kerr, B., Neuhauser, C., Bohannan, B. et al. Local migration promotes competitive restraint in a host–pathogen 'tragedy of the commons'. Nature 442, 75–78 (2006).

Download citation

  • Received:

  • Accepted:

  • 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