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:

Geographic structure and dynamics of coevolutionary selection

Abstract

Coevolution of species is one of the major processes organizing the Earth's biodiversity. Recent coevolutionary theory has indicated that the geographic structure of species has the potential to impose powerful and continuing effects on coevolutionary dynamics, if that structure creates selection mosaics and coevolutionary hotspots across landscapes1,2,3,4,5,6,7. Here we confirm that current coevolutionary selection in interspecific interactions can be highly divergent across both narrow and broad geographic scales, thereby fuelling continuing coevolution of taxa. Study of a widespread plant–insect interaction across a broad range of habitats for several years showed that an insect functioning both as a pollinator and a floral parasite can be strongly mutualistic in some habitats but commensal or antagonistic in neighbouring habitats. The results for one of the habitats span seven years, demonstrating that the local structure of coevolutionary selection can remain stable across multiple generations. Conservation of the evolutionary processes maintaining long-term biological diversity may require preservation of the conditions that allow a long-term shifting geographic mosaic of coevolutionary hotspots and coldspots.

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: Distribution of study sites for analysis of coevolutionary hotspots in the interaction between the plant Lithophragma parviflorum and the moth Greya politella.

Similar content being viewed by others

References

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

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. 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 

  4. Case, T. J. & Taper, M. L. Interspecific competition, environmental gradients, gene flow, and the coevolution of species' borders. Am. Nat. 155, 583–605 (2000)

    Article  CAS  Google Scholar 

  5. 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 

  6. Hochberg, M. E., Gomulkiewicz, R., Holt, R. D. & Thompson, J. N. Weak sinks could cradle mutualisms—strong sources should harbour parasitic symbioses. J. Evol. Biol. 13, 213–222 (2000)

    Article  Google Scholar 

  7. Nuismer, S. L., Thompson, J. N. & Gomulkiewicz, R. Coevolutionary clines across selection mosaics. Evolution 54, 1102–1115 (2000)

    Article  CAS  Google Scholar 

  8. Holland, J. N. & Fleming, T. H. Geographic and population variation in pollinating seed-consuming interactions between senita cacti (Lophocereus schottii) and senita moths (Upiga virescens). Oecologia 121, 405–410 (1999)

    Article  ADS  CAS  Google Scholar 

  9. Berenbaum, M. & Zangerl, A. Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl Acad. Sci. USA 95, 13743–13748 (1998)

    Article  ADS  CAS  Google Scholar 

  10. Benkman, C. W. The selection mosaic and diversifying coevolution between crossbills and lodgepole pine. Am. Nat. 153, S75–S91 (1999)

    Article  Google Scholar 

  11. Benkman, C. W., Holimon, W. C. & Smith, J. W. The influence of a competitor on the geographic mosaic of coevolution between crossbills and lodgepole pine. Evolution 55, 282–294 (2001)

    Article  CAS  Google Scholar 

  12. Brodie, E. D. III & Brodie, E. D. Jr Costs of exploiting poisonous prey: evolutionary trade-offs in a predator-prey arms race. Evolution 53, 626–631 (1999)

    Article  Google Scholar 

  13. Burdon, J. J. & Thrall, P. H. Spatial and temporal patterns in coevolving plant and pathogen associations. Am. Nat. 153, S15–S33 (1999)

    Article  CAS  Google Scholar 

  14. Kraaijeveld, A. R. & Godfray, H. C. J. Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. Am. Nat. 153, S61–S74 (1999)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. Radtkey, R. R., Fallon, S. M. & Case, T. J. Character displacement in some Cnemidophorus lizards revisited: A phylogenetic analysis. Proc. Natl Acad. Sci. USA 94, 9740–9745 (1997)

    Article  ADS  CAS  Google Scholar 

  17. Parker, M. A. Mutualism in metapopulations of legumes and rhizobia. Am. Nat. 153, S48–S60 (1999)

    Article  Google Scholar 

  18. De Jong, P. W., De Vos, H. & Nielsen, J. K. Demic structure and its relation with the distribution of an adaptive trait in Danish flea beetles. Mol. Ecol. 10, 1323–1332 (2001)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  20. Thompson, J. N. & Pellmyr, O. Mutualism with pollinating seed parasites amid co-pollinators: constraints on specialization. Ecology 73, 1780–1791 (1992)

    Article  Google Scholar 

  21. Pellmyr, O. & Thompson, J. N. Sources of variation in pollinator contribution within a guild: the effects of plant and pollinator factors. Oecologia 107, 595–604 (1996)

    Article  ADS  Google Scholar 

  22. Caicco, S. L., Scott, J. M., Butterfield, B. & Csuti, B. A gap analysis of the management status of the vegetation of Idaho (U.S.A.). Conserv. Biol. 9, 498–511 (1995)

    Article  Google Scholar 

  23. Ricketts, T. H., Dinerstein, E., Olson, D. M. & Loucks, C. J. (eds) Terrestrial Ecoregions of North America: A Conservation Assessment (Island Press, Washington DC, 1999)

  24. Pellmyr, O., Thompson, J. N., Brown, J. M. & Harrison, R. G. Evolution of pollination and mutualism in the yucca moth lineage. Am. Nat. 148, 827–847 (1996)

    Article  Google Scholar 

  25. Pellmyr, O. & Thompson, J. N. Multiple occurrences of mutualism in the yucca moth lineage. Proc. Natl Acad. Sci. USA 89, 2927–2929 (1992)

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Althoff, E. Bartlett, R. Beck, N. Bonilla, S. Bradford, C. Clark, C. Cody, M. Jacoby, S. Lambert, Y. Martinez, K. Merg, S. Nuismer, J. Olmstead, S. Ringo, K. Segraves, D. Shepard, Z. Stanley and T. Steury for help in the field or laboratory, and R. Calsbeek, D. Hembry, K. Horjus, R. Hufft, N. Janz, K. Merg, S. Nuismer and J. Richardson for helpful discussions on the manuscript. We are grateful for permissions from the Clearwater, Nez Perce, Payette, Salmon, and Umatilla National Forests and from the Turnbull National Wildlife Refuge. This work was supported by the NSF.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John N. Thompson.

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

Thompson, J., Cunningham, B. Geographic structure and dynamics of coevolutionary selection. Nature 417, 735–738 (2002). https://doi.org/10.1038/nature00810

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature00810

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

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