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.

  • Letter
  • Published:

The effect of migration on local adaptation in a coevolving host–parasite system

Nature volume 437, pages 253–256 (2005)Cite this article

Abstract

Antagonistic coevolution between hosts and parasites in spatially structured populations can result in local adaptation of parasites1,2,3,4,5; that is, the greater infectivity of local parasites than foreign parasites on local hosts1. Such parasite specialization on local hosts has implications for human health and agriculture. By contrast with classic single-species population-genetic models6,7, theory indicates that parasite migration between subpopulations might increase parasite local adaptation, as long as migration does not completely homogenize populations8,9,10,11. To test this hypothesis we developed a system-specific mathematical model and then coevolved replicate populations of the bacterium Pseudomonas fluorescens and a parasitic bacteriophage with parasite only, with host only or with no migration. Here we show that patterns of local adaptation have considerable temporal and spatial variation and that, in the absence of migration, parasites tend to be locally maladapted. However, in accord with our model, parasite migration results in parasite local adaptation, but host migration alone has no significant effect.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: The simulated effect of differential migration rates on local adaptation.
Figure 2: The effect of differential migration rates on local adaptation.
Figure 3: Mean local adaptation of parasites.
Figure 4: Mean parasite infectivity.

Similar content being viewed by others

References

  1. Kawecki, T. D. & Ebert, D. Conceptual issues in local adaptation. Ecol. Lett. 7, 1225–1241 (2004)

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  3. Kaltz, O. & Shykoff, J. A. Local-adaptation in host–parasite systems. Heredity 81, 361–370 (1998)

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Thompson, J. N. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 153, S1–S14 (1999)

    Article  Google Scholar 

  6. Slatkin, M. Gene flow and the genetic structure of natural populations. Science 236, 787–792 (1987)

    Article  ADS  CAS  Google Scholar 

  7. Lenormand, T. Gene flow and the limits to natural selection. Trends Ecol. Evol. 17, 183–189 (2002)

    Article  Google Scholar 

  8. Gandon, S., Capowiez, Y., Dubois, 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 

  9. Lively, C. M. Migration, virulence and the geographic mosaic of adaptation by parasites. Am. Nat. 153, S34–S47 (1999)

    Article  CAS  Google Scholar 

  10. 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 

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

    Article  Google Scholar 

  12. Parker, M. A. Local population differentiation for compatability in an annual legume and its host-specific fungal pathogen. Evolution 39, 713–723 (1985)

    Article  Google Scholar 

  13. Lively, C. M. Adaptation by a parasitic trematode to local populations of its host. Evolution 46, 1663–1671 (1989)

    Article  Google Scholar 

  14. Lively, C. M. & Dybdahl, M. F. Parasite adaptation to locally common host genotypes. Nature 405, 679–681 (2000)

    Article  ADS  CAS  Google Scholar 

  15. McCoy, K. D., Boulinier, T., Schjorring, S. & Michalakis, Y. Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evol. Ecol. Res. 4, 441–456 (2002)

    Google Scholar 

  16. Kaltz, O., Gandon, S., Michalakis, Y. & Shykoff, J. A. Local maladaptation in the anther-smut fungus Microbortyum violaceum to its host Silene latifolia: Evidence from a cross inoculation experiment. Evolution 53, 395–407 (1999)

    PubMed  Google Scholar 

  17. Mutikainen, P., Salonen, V., Puustinen, S. & Koskela, T. Local adaptation, resistance, and virulence in a hemiparasitic plant–host plant interaction. Evolution 54, 433–440 (2000)

    CAS  PubMed  Google Scholar 

  18. Oppliger, A., Vernet, R. & Baez, M. Parasite local maladaptation in the Canarian lizard Gallotia galloti (Reptilia: Lacertidae) parasitized by haemogregarian blood parasite. J. Evol. Biol. 12, 951–955 (1999)

    Article  Google Scholar 

  19. 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 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  Google Scholar 

  22. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long term experimental evolution in Escherichia coli. 1. Adaptation and divergence during 2000 generations. Am. Nat. 138, 1315–1341 (1991)

    Article  Google Scholar 

  23. Agrawal, A. & Lively, C. M. Infection genetics: gene-for-gene versus matching-alleles models and all points in between. Evol. Ecol. Res. 4, 79–90 (2002)

    Google Scholar 

  24. Frank, S. A. Statistical properties of polymorphism in host–parasite genetics. Evol. Ecol. 10, 307–317 (1996)

    Article  Google Scholar 

  25. Morand, S., Manning, S. D. & Woolhouse, M. E. J. Parasite–host coevolution and geographic patterns of parasite infectivity and host susceptibility. Proc. R. Soc. Lond. B 263, 119–128 (1996)

    Article  ADS  CAS  Google Scholar 

  26. Crawley, M. J. GLIM for Ecologists (Blackwell Science, Oxford, 1993)

    Google Scholar 

  27. Lenski, R. E. Coevolution of bacteria and phage—are there endless cycles of bacterial defenses and phage counterdefenses? J. Theor. Biol. 108, 319–325 (1984)

    Article  CAS  Google Scholar 

  28. Miralles, R., Moya, A. & Elena, S. F. Effect of poulation patchiness and migration rates on the adaptation and divergence of vesicular stomatitis virus quasispecies populations. J. Gen. Virol. 80, 2051–2059 (1999)

    Article  CAS  Google Scholar 

  29. Rainey, P. B. & Bailey, M. J. Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome. Mol. Microbiol. 19, 521–533 (1996)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Brockhurst, T. Day, F. Harrison, O. Kaltz, C. Lively and his group, Y. Michalakis, I. Olivieri, L. Lopez Pascua and A. Rivero for comments on the manuscript. This work was funded by the Royal Society.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Oxford, South Parks Road, OX1 3PS, Oxford, UK

    Andrew D. Morgan & Angus Buckling

  2. Génétique et Évolution des Maladies Infectieuses, UMR CNRS/IRD 2724, IRD, 911 avenue Agropolis, 34394 Cedex 5, Montpellier, France

    Sylvain Gandon

Authors
  1. Andrew D. Morgan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sylvain Gandon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Angus Buckling
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew D. Morgan.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

The Supplementary Notes contains a discussion of different measures of local adaptation (including Fig. S1) and details of the model formulation and results (including a table and Fig. S2). (DOC 268 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Morgan, A., Gandon, S. & Buckling, A. The effect of migration on local adaptation in a coevolving host–parasite system. Nature 437, 253–256 (2005). https://doi.org/10.1038/nature03913

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03913

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