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:

Three-butterfly system provides a field test of müllerian mimicry

Nature volume 409, pages 338–340 (2001)Cite this article

Abstract

In 1879, Müller proposed that two brightly coloured distasteful butterfly species (co-models) that share a single warning-colour pattern would benefit by spreading the selective burden of educating predators1,2,3,4,5. The mutual benefit of sharing warning signals among distasteful species, so-called müllerian mimicry, is supported by comparative evidence2,3, theoretical studies5,6 and laboratory simulations7; however, to date, this key exemplar of adaptive evolution has not been experimentally tested in the field. To measure natural selection generated by müllerian mimicry, I exploited the unusual polymorphism of Heliconius cydno (Lepidoptera: Nymphalidae)8. Here I show increased survival of H. cydno morphs that match locally abundant monomorphic co-model species. This study demonstrates müllerian mimicry in the field. It also shows that müllerian mimicry with several co-models generates geographically divergent selection, which explains the existence of polymorphism in distasteful species with warning coloration9.

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: Experimental designs of aposematic selection and müllerian mimicry in Heliconius butterflies.
Figure 2: Observed proportion (log10 scale) of control and experimental H. cydno butterflies resighted after initial release.
Figure 3: Probability of establishment (PE) versus exponential death rates (λ) estimated for released butterflies at low-density sites Manta Real, Agua Caliente and Tinalandia summed (a), and at all sites combined (b).

Similar content being viewed by others

References

  1. Müller, F. Ituna and Thyridia; a remarkable case of mimicry in butterflies. Trans. Ent. Soc. Lond. 1879, xx– xxix (1879).

    Google Scholar 

  2. Wickler, W. Mimicry in Plants and Animals (Wiedenfield and Nicolson, London, 1968).

    Google Scholar 

  3. Turner, J. R. G. Butterfly mimicry—the genetical evolution of an adaptation. Evol. Biol. 10, 163–206 (1977).

    Google Scholar 

  4. Fisher, R. A. The Genetical Theory of Natural Selection (Dover Publications, New York, 1958).

    MATH  Google Scholar 

  5. Holmgren, N. M. & Enquist, M. Dynamics of mimicry evolution. Biol. J. Linn. Soc. 66, 145– 158 (1999).

    Article  Google Scholar 

  6. Gavrilets, S. & Hastings, A. Coevolutionary chase in two-species systems with applications to mimicry. J. Theor. Biol. 191, 415–427 (1998).

    Article  CAS  PubMed  Google Scholar 

  7. Alatalo, R. & Mappes, J. Tracking the evolution of warning signals. Nature 382, 708– 710 (1996).

    Article  ADS  CAS  Google Scholar 

  8. Kapan, D. D. Divergent Natural Selection and Müllerian Mimicry in Polymorphic Heliconius cydno (Lepidoptera: Nymphalidae). Thesis, Univ. of British Columbia (1998).

    Google Scholar 

  9. Joron, M. & Mallet, J. L. Diversity in mimicry: paradox or paradigm. Trends Ecol. Evol. 13, 461– 466 (1998).

    Article  CAS  Google Scholar 

  10. Benson, W. W. Natural selection for Müllerian mimicry in Heliconius erato in Costa Rica. Science 176, 936– 939 (1972).

    Article  ADS  CAS  Google Scholar 

  11. Mallet, J. L. & Barton, N. H. Strong natural selection in a warning-colour hybrid zone. Evolution 43, 421–431 (1989).

    Article  Google Scholar 

  12. Endler, J. A. Frequency-dependent predation, crypsis and aposematic coloration. Phil. Trans. R. Soc. Lond. B 319, 459– 472 (1988).

    Article  Google Scholar 

  13. Gilbert, L. E. in Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Region (eds Lewinsohn, P. W., Wilson, T. M., Fernandes, G. & Benson, W. W.) 403–427 (John Wiley and Sons, New York, 1991).

    Google Scholar 

  14. Brower, L. P., Brower, J. V. Z. & Collins, C. T. Experimental studies of mimicry. 7. Relative palatability and Müllerian mimicry among Neotropical butterflies of the subfamily Heliconiinae. Zoologica 48, 65– 83 (1963).

    Google Scholar 

  15. Chai, P. Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rainforest. Biol. J. Linn. Soc. 29, 161– 189 (1986).

    Article  Google Scholar 

  16. Brower, L. P., Cook, L. M. & Croze, H. J. Predator responses to artificial Batesian mimics released in a neotropical environment. Evolution 21 , 11–23 (1967).

    Article  PubMed  Google Scholar 

  17. Cook, L. M., Brower, L. & Alcock, P. J. An attempt to verify mimetic advantage in a neotropical environment. Evolution 23, 339– 345 (1969).

    Article  PubMed  Google Scholar 

  18. Waldbauer, G. P. & Sternburg, J. G. Saturniid moths as mimics: an alternative interpretation of attempts to demonstrate mimetic advantage in nature. Evolution 29, 650–658 (1975).

    Article  CAS  PubMed  Google Scholar 

  19. Edwards, A. W. F. Likelihood 2nd edn (Johns Hopkins Univ. Press, Baltimore, 1992).

    MATH  Google Scholar 

  20. Akaike, H. in International Symposium on Information Theory 2nd edn (eds Petran, B. N. & Csáki, F.) 267–281 (Akadémiai Kiadi, Budapest, 1973).

    Google Scholar 

  21. Lebreton, J. D., Burnham, K. P., Clobert, J. & Anderson, D. R. Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol. Monogr. 62, 67–118 (1992).

    Article  Google Scholar 

  22. Dunlap-Pianka, H., Boggs, C. L. & Gilbert, L. E. Ovarian dynamics in heliconiine butterflies: programmed senescence versus eternal youth. Science 197, 487–490 (1977).

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Brown, K. & Benson, W. W. Adaptive polymorphism associated with multiple Müllerian mimicry in Heliconius numata (Lepid. Nymph.). Biotropica 6, 205–228 (1974).

    Article  Google Scholar 

  24. Mallet, J. L. & Joron, M. Evolution of diversity in warning colour and mimicry: Polymorphisms, shifting balance, and speciation. Annu. Rev. Ecol. Syst. 30, 201–233 (2000).

    Article  Google Scholar 

  25. Mallet, J. L. Mallet & Singer, M. C. Individual selection, kin selection, and the shifting balance in the evolution of warning colours: the evidence from butterflies. Biol. J. Linn. Soc. 32, 337–350 (1987).

    Article  Google Scholar 

  26. Turner, J. R. & Mallet, J. L. Did forest islands drive the diversity of warningly coloured butterflies? Biotic drift and the shifting balance. Phil. Trans. R. Soc. Lond. B 351, 835– 845 (1996).

    Article  ADS  Google Scholar 

  27. Mallet, J. L., McMillan,W. & Jiggins, C. in Endless Forms: Species and Speciation (eds Berlocher, S. & Howard, D.) 390–403 (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  28. Mallet, J. L., Longino, J. T., Murawski, D., Murawski, A. & Gamboa, A. S. Handling effects in Heliconius : Where do all the butterflies go? J. Anim. Ecol. 56, 377–386 (1987).

    Article  Google Scholar 

  29. Skalski, J. R., Hoffman, A. & Smith, S. G. in Marked Individuals in the Study of Bird Populations (eds Lebreton, J. D. & North, P. M.) 9–28 (Birkhauser, Basel, 1993).

    Google Scholar 

  30. Mallet, J. L. et al. Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in Heliconius hybrid zones. Genetics 124, 921 –936 ( 1990).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I thank D. Schluter, L. Gilbert, M. Kirkpatrick, M. Singer, R. Dudley, U. Mueller, P. Schappert, W. O. McMillan and S. Bennett for valuable discussion and critical review of this manuscript, and H. Knechtel, C. Chapman, J. Page, S. Zaklan and K. Holston for field assistance. This research is supported by Earthwatch and its volunteer corps, by L. Gilbert and, in part, by a National Science and Engineering Research Council grant to D. Schluter.

Author information

Author notes

  1. Durrell D. Kapan

    Present address: Departemento de Biologia, Universidad de Puerto Rico—Rio Piedras, San Juan, 00931-3360, Puerto Rico

  2. Correspondence and requests for materials should be addressed to the author.

Authors and Affiliations

    Authors
    1. Durrell D. Kapan
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Durrell D. Kapan.

    Additional information

    Centre for Biodiversity Research, Department of Zoology, University of British Colombia, Vancouver, BC, V6T 1Z4, Canada, and Section of Integrative Biology, Patterson Laboratories, University of Texas, Austin, Texas 78712-1064, USA

    Rights and permissions

    Reprints and permissions

    About this article

    Cite this article

    Kapan, D. Three-butterfly system provides a field test of müllerian mimicry . Nature 409, 338–340 (2001). https://doi.org/10.1038/35053066

    Download citation

    • Received:

    • Accepted:

    • Issue Date:

    • DOI: https://doi.org/10.1038/35053066

    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