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.

Adaptation varies through space and time in a coevolving host–parasitoid interaction


One of the central challenges of evolutionary biology is to understand how coevolution organizes biodiversity over complex geographic landscapes. Most species are collections of genetically differentiated populations, and these populations have the potential to become adapted to their local environments in different ways. The geographic mosaic theory of coevolution incorporates this idea by proposing that spatial variation in natural selection and gene flow across a landscape can shape local coevolutionary dynamics1,2,3,4,5,6,7. These effects may be particularly strong when populations differ across productivity gradients, where gene flow will often be asymmetric among populations8. Conclusive empirical tests of this theory have been particularly difficult to perform because they require knowledge of patterns of gene flow, historical population relationships and local selection pressures2. We have tested these predictions empirically using a model community of bacteria and bacteriophage (viral parasitoids of bacteria). We show that gene flow across a spatially structured landscape alters coevolution of parasitoids and their hosts and that the resulting patterns of adaptation can fluctuate in both space and time.

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

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: The experimental landscapes.
Figure 2: Adaptation in the bacteriophage populations from each productivity level.
Figure 3: Variation of the adaptation ratio.


  1. Thompson, J. N. The Coevolutionary Process (Univ. of Chicago Press, Chicago, 1994)

    Book  Google Scholar 

  2. Brodie, E. D. Jr, Ridenhour, B. J. & Brodie, E. D. III The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56, 2067–2082 (2002)

    Article  Google Scholar 

  3. Burdon, J. J. & Thrall, P. H. Spatial and temporal patterns in coevolving plant and pathogen associations. Am. Nat. 153, S15–S33 (2002)

    Article  Google Scholar 

  4. Zangerl, A. R. & Berenbaum, M. R. Phenotype matching in wild parsnip and parsnip webworms: causes and consequences. Evolution 57, 806–815 (2003)

    Article  CAS  Google Scholar 

  5. Thompson, J. N. & Cunningham, B. M. Geographic structure and dynamics of coevolutionary selection. Nature 417, 735–738 (2002)

    Article  CAS  ADS  Google Scholar 

  6. Benkman, C. W., Parchman, T. L., Favis, A. & Siepielski, A. M. Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. Am. Nat. 162, 182–194 (2003)

    Article  Google Scholar 

  7. Nuismer, S. L., Thompson, J. N. & Gomulkiewicz, R. Gene flow and geographically structured coevolution. Proc. R. Soc. Lond. B 266, 605–609 (1999)

    Article  Google Scholar 

  8. Hochberg, M. & van Baalen, M. Antagonistic coevolution over productivity gradients. Am. Nat. 152, 620–634 (1998)

    Article  CAS  Google Scholar 

  9. Chao, L., Levin, B. R. & Stewart, F. M. A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology 58, 369–378 (1977)

    Article  Google Scholar 

  10. 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 

  11. Shrag, S. J. & Mittler, J. E. Host–parasite coexistence: the role of spatial refuges in stabilizing bacteria-phage interactions. Am. Nat. 148, 348–377 (1996)

    Article  Google Scholar 

  12. Bohannan, B. J. M. & Lenski, R. E. The relative importance of competition and predation varies with productivity in a model system. Am. Nat. 156, 329–340 (2000)

    Article  Google Scholar 

  13. Buckling, A. & Rainey, P. B. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. Lond. B 269, 931–936 (2002)

    Article  Google Scholar 

  14. Thompson, J. N. The evolution of species interactions. Science 284, 2116–2118 (1999)

    Article  CAS  Google Scholar 

  15. Bohannan, B. J. M. & Lenski, R. E. The effect of resource enrichment on a chemostat community of bacteria and phage. Ecology 78, 2303–2315 (1997)

    Article  Google Scholar 

  16. Gandon, S. Local adaptation and the geometry of host–parasite coevolution. Ecol. Lett. 5, 246–256 (2002)

    Article  Google Scholar 

  17. Gandon, S. & Michalakis, Y. Local adaptation, evolutionary potential and host–parasite coevolution: interactions between migration, mutation, population size and generation time. J. Evol. Biol. 15, 451–462 (2002)

    Article  Google Scholar 

  18. Gomulkiewicz, R., Thompson, J. N., Holt, R. D., Nuismer, S. L. & Hochberg, M. E. Hot spots, cold spots and the geographic mosaic theory of coevolution. Am. Nat. 156, 156–174 (2000)

    Article  Google Scholar 

  19. Slatkin, M. Gene flow in natural populations. Annu. Rev. Ecol. Syst. 16, 393–430 (1985)

    Article  Google Scholar 

  20. Futuyma, D. J. Evolutionary Biology, 3rd edn (Sinauer Associates Inc., Sunderland, 1998)

    Google Scholar 

  21. Gandon, S., Capowiez, Y., Dubios, Y., Michalakis, Y. & Olivieri, I. Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc. R. Soc. Lond. B 263, 1003–1009 (1996)

    Article  ADS  Google Scholar 

  22. Buckling, A., Wills, M. A. & Colegrave, N. Adaptation limits diversification of experimental bacterial populations. Science 302, 2107–2109 (2003)

    Article  CAS  ADS  Google Scholar 

  23. Brockhurst, M. A., Morgan, A. D., Rainey, P. B. & Buckling, A. Population mixing accelerates coevolution. Ecol. Lett. 6, 975–979 (2003)

    Article  Google Scholar 

  24. Bohannan, B. J. M. & Lenski, R. E. Effect of prey heterogeneity on the response of a model food chain to resource enrichment. Am. Nat. 153, 73–82 (1999)

    Article  Google Scholar 

  25. Rice, W. R. Analyzing tables of statistical tests. Evolution 43, 223–225 (1989)

    Article  Google Scholar 

Download references


We thank B. Kerr, E. Danner and members of the Thompson and Bohannan laboratories for comments on previous drafts of this manuscript. We are grateful to P. Raimondi for assistance with data analysis.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Samantha E. Forde.

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

Forde, S., Thompson, J. & Bohannan, B. Adaptation varies through space and time in a coevolving host–parasitoid interaction. Nature 431, 841–844 (2004).

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