Parasite adaptation to locally common host genotypes (original) (raw)

Nature volume 405, pages 679–681 (2000)Cite this article

Abstract

According to the Red Queen hypothesis—which states that interactions among species (such as hosts and parasites) lead to constant natural selection for adaptation and counter-adaptation—the disproportionate evolutionary success of parasites on common host genotypes leads to correlated selection for sexual reproduction1,2,3,4,5,6,7,8 and local adaptation by the parasite population9,10,11,12,13,14. Here we determined whether local adaptation is due to disproportionate infection of common host genotypes, and, if so, whether infection of common host genotypes is due to commonness per se, or some other aspect of these genotypes. In a reciprocal cross-inoculation experiment parasites occupying the same geographical area (sympatric) infected locally common host genotypes significantly more often than rare host genotypes, whereas parasites occupying separate geographical areas (allopatric) showed no such significant difference. A mixed source of parasites (containing F1 hybrids) also showed no difference in infection between rare and common host genotypes. These results show that local adaptation results from parasite tracking of locally common host genotypes, and, as such, a necessary condition of the Red Queen hypothesis is met.

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

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

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

Additional access options:

Similar content being viewed by others

References

  1. Jaenike, J. An hypothesis to account for the maintenance of sex within populations. Evol. Theor. 3,191–194 (1978).
  2. Bremermann, H. J. Sex and polymorphism as strategies in host–pathogen interactions. J. Theor. Biol. 87, 671–702 (1980).
    Article MathSciNet CAS Google Scholar
  3. Hamilton, W. D. Sex versus non-sex versus parasite. Oikos 35, 282–290 (1980).
    Article Google Scholar
  4. Seger, J. & Hamilton, W. D. in The Evolution of Sex (eds Michod, R. E. & Levin, B. R.) 176–193 (Sinauer and Associates, Sunderland, 1988).
    Google Scholar
  5. Nee, S. Antagonistic coevolution and the evolution of genotype randomization. J. Theor. Biol. 140, 499–518 ( 1989).
    Article MathSciNet CAS Google Scholar
  6. Hamilton, W. D., Axelrod, R. & Tanese, R. Sexual reproduction as an adaptation to resist parasites (A review). Proc. Natl Acad. Sci. USA 87, 3566–3573 (1990).
    Article ADS CAS Google Scholar
  7. Howard, R. S. & Lively, C. M. Parasitism, mutation accumulation and the maintenance of sex. Nature 367, 554–557 (1994).
    Article ADS CAS Google Scholar
  8. Peters, A. D. & Lively, C. M. The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. Am. Nat. 154, 393–405 ( 1999).
    Article CAS Google Scholar
  9. Judson, O. P. Preserving genes: a model of the maintenance of genetic variation in a metapopulation under frequency-dependent selection. Genetic. Res. 65, 175–191 (1995).
    Article Google Scholar
  10. Gandon, S., Capoweiz, Y., Dubois, Y., Michalakis, Y. & Olivieri, I. Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc. R. Soc. B 263, 1003–1009 (1996).
    Article ADS Google Scholar
  11. Lively, C. M. Migration, virulence, and the geographic mosaic of adaptation by parasites. Am. Nat. 153, S34–S47 (1999).
    Article CAS Google Scholar
  12. Parker, M. Local population differentiation for compatibility 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. Ebert, D. Virulence and local adaptation of a horizontally transmitted parasite. Science 256, 1084–1086 ( 1994).
    Article ADS Google Scholar
  15. Dybdahl, M. D. & Lively, C. M. Diverse, endemic and polyphyletic clones in mixed populations of the freshwater snail Potamopyrgus antipodarum. J. Evol. Biol. 8, 385– 398 (1995).
    Article Google Scholar
  16. Dybdahl, M. F. & Lively, C. M. Host–parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evolution 52, 1057– 1066 (1998).
    Article Google Scholar
  17. Dybdahl, M. F. & Lively, C. M. The geography of coevolution: comparative population structures for a snail and its trematode parasite. Evolution 50, 2264– 2275 (1996).
    Article Google Scholar
  18. Norusis, M. J. SPSS Advanced Statistics User's Guide (SPSS, Chicago, 1990).
    Google Scholar

Download references

Acknowledgements

We thank L. Delph for helpful comments on the manuscript. This study was supported by the US National Science Foundation.

Author information

Author notes

  1. Mark F. Dybdahl
    Present address: Department of Biological Sciences, Ohio University, Athens, Ohio, 45701, USA
  2. Curtis M. Lively, Mark F. Dybdahl: Correspondence and requests for materials should be addressed

Authors and Affiliations

  1. Department of Biology, Indiana University, Bloomington , 47405-3700, Indiana, USA
    Curtis M. Lively & Mark F. Dybdahl
  2. Department of Biological Sciences, Ohio University, Athens, Ohio, 45701, USA
    Curtis M. Lively

Authors

  1. Curtis M. Lively
    You can also search for this author inPubMed Google Scholar
  2. Mark F. Dybdahl
    You can also search for this author inPubMed Google Scholar

Corresponding authors

Correspondence toCurtis M. Lively or Mark F. Dybdahl.

Rights and permissions

About this article

Cite this article

Lively, C., Dybdahl, M. Parasite adaptation to locally common host genotypes.Nature 405, 679–681 (2000). https://doi.org/10.1038/35015069

Download citation