Abstract
Speciation is facilitated if ecological adaptation directly causes assortative mating1, but few natural examples are known. Here we show that a shift in colour pattern mimicry was crucial in the origin of two butterfly species. The sister species Heliconius melpomene and Heliconius cydno recently diverged to mimic different model taxa, and our experiments show that their mimetic coloration is also important in choosing mates. Assortative mating between the sister species means that hybridization is rare in nature, and the few hybrids that are produced are non-mimetic, poorly adapted intermediates. Thus, the mimetic shift has caused both pre-mating and post-mating isolation. In addition, individuals from a population of H. melpomene allopatric to H. cydno court and mate with H. cydno more readily than those from a sympatric population. This suggests that assortative mating has been enhanced in sympatry.
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
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Maynard Smith, J. Sympatric speciation. Am. Nat. 100, 637–650 (1966).
Bates, H. W. Contributions to an insect fauna of the Amazon valley. Lepidoptera: Heliconidae. Trans. Linn. Soc. Lond. 23, 495–566 (1862).
Vane-Wright, R. I. in Diversity of Insect Faunas (eds Mound, L. A. & Waloff, N.) 56–70 (Blackwell Scientific, Oxford, 1978).
Turner, J. R. G. Adaptation and evolution in Heliconius: a defense of neo-Darwinism. Annu. Rev. Ecol. Syst. 12, 99–121 (1981).
Mallet, J. & Joron, M. Evolution of diversity in warning colour and mimicry: Polymorphisms, shifting balance and speciation. Annu. Rev. Ecol. Syst. 30, 201–233 (1999).
Turner, J. R. G. Adaptive radiation and convergence in subdivisions of the butterfly genus Heliconius (Lepidoptera: Nymphalidae). Zool. J. Linn. Soc. 58, 297–308 (1976).
McMillan, W. O., Jiggins, C. D. & Mallet, J. What initiates speciation in passion vine butterflies? Proc. Natl Acad. Sci. USA 94, 8628–8633 (1997).
Mallet, J., McMillan, W. O. & Jiggins, C. D. in Endless Forms: Species and Speciation (eds Howard, D. J. & Berlocher, S. H.) 390–403 (Oxford Univ. Press, New York, 1998).
Linares, M. Adaptive Microevolution Through Hybridization and Biotic Destruction in the Neotropics (Thesis, Univ. Texas, Austin, Texas, 1989).
Gilbert, L. E. in Ecology and Evolution Taking Flight: Butterflies as Model Systems (eds Boggs, C. L., Watt, W. B. & Ehrlich, P. R.) (Univ. Chicago Press, Chicago, Illinois, in the press).
Brower, A. V. Z. Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution 50, 195–221 (1996).
Mallet, J. Causes and consequences of a lack of coevolution in Müllerian mimicry. Evol. Ecol. 13, 777–806 (1999).
Dobzhansky, T. Speciation as a stage in evolutionary divergence. Am. Nat. 74, 312–321 (1940).
Butlin, R. Speciation by reinforcement. Trends Ecol. Evol. 2, 8–12 (1987).
Noor, M. A. F. Reinforcement and other consequences of sympatry. Heredity 83, 503–508 (1999).
Mallet, J. & Barton, N. H. Strong natural selection in a warning color hybrid zone. Evolution 43, 421–431 (1989).
Dieckmann, U. & Doebeli, M. On the origin of species by sympatric speciation. Nature 400, 354–357 (1999).
Kirkpatrick, M. Reinforcement and divergence under assortative mating. Proc. Roy. R. Lond. B 267, 1649–1655 (2000).
Craig, T. P., Itami, J. K., Abrahamson, W. G. & Horner, J. D. Behavioral evidence for host-race formation in Eurosta solidaginis. Evolution 47, 1696–1710 (1993).
Feder, J. L. et al. Host fidelity is an effective premating barrier between sympatric races of the apple maggot fly. Proc. Natl Acad. Sci. USA 91, 7990–7994 (1994).
Rundle, H. D., Nagel, L., Wenrick Boughman, J. & Schluter, D. Natural selection and parallel speciation in sympatric sticklebacks. Science 287, 306–308 (2000).
Mallet, J. & Gilbert, L. E. Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. Biol. J. Linn. Soc. 55, 159–180 (1995).
Edwards, A. W. F. Likelihood (Cambridge Univ. Press, Cambridge, 1972).
Acknowledgements
We thank C. Paresce, C. Estrada, R. Woods, M. Beltrán and L. O'Donovan for help with experiments; B. Hermiers for help in French Guiana; F. Jiggins, M. Joron, I. Emelianov, E. Bermingham and G. Hurst for discussion; and S. Upson at Perkin Elmer for reflectance measurements. This work was carried out with permission from ANAM (Autoridad Nacional del Ambiente) to work in the República de Panamá, and was funded by the Natural Environment Research Council and a BBSRC (Biotechnology and Biological Sciences Research Council) studentship.
Author information
Authors and Affiliations
Corresponding author
Supplementary information
Rights and permissions
About this article
Cite this article
Jiggins, C., Naisbit, R., Coe, R. et al. Reproductive isolation caused by colour pattern mimicry. Nature 411, 302–305 (2001). https://doi.org/10.1038/35077075
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/35077075
This article is cited by
-
Beyond color and pattern: elucidating the factors associated with intraspecific aggression in the mimic poison frog (Ranitomeya imitator)
Evolutionary Ecology (2024)
-
Heliconiini butterflies as a case study in evolutionary cognitive ecology: behavioural innovation and mushroom body expansion
Behavioral Ecology and Sociobiology (2023)
-
Evaluation of trap efficiency for the Asian longhorned beetle, Anoplophora glabripennis
Journal of Forestry Research (2023)
-
Reproductive behaviors promote ecological and phenotypic sexual differentiation in the critically endangered Lehmann’s poison frog
Evolutionary Ecology (2022)
-
The evolution of opsin genes in five species of mirid bugs: duplication of long-wavelength opsins and loss of blue-sensitive opsins
BMC Ecology and Evolution (2021)
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.