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

Abstract

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.

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

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Acknowledgements

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.

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Correspondence to Benjamin Kerr.

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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)

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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). https://doi.org/10.1038/nature04864

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