Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-26T06:56:56.966Z Has data issue: false hasContentIssue false

10 - Rapid speciation, hybridization and adaptive radiation in the Heliconius melpomene group

Published online by Cambridge University Press:  05 June 2012

By
James Mallet
Edited by
Roger Butlin ,
Jon Bridle  and
Dolph Schluter
James Mallet
Affiliation:
Galton Laboratory, Department of Biology, University College London
Roger Butlin
Affiliation:
University of Sheffield
Jon Bridle
Affiliation:
University of Bristol
Dolph Schluter
Affiliation:
University of British Columbia, Vancouver
Get access

Summary

In 1998 it seemed clear that a pair of ‘sister species’ of tropical butterflies, Heliconius melpomene and Heliconius cydno persisted in sympatry in spite of occasional although regular hybridization. They speciated and today can coexist as a result of ecological divergence. An important mechanism in their speciation was the switch in colour pattern between different Müllerian mimicry rings, together with microhabitat and host-plant shifts, and assortative mating produced as a side effect of the colour pattern differences. An international consortium of Heliconius geneticists has recently been investigating members of the cydno superspecies, which are in a sense the ‘sisters’ of one of the original ‘sister species’, cydno. Several of these locally endemic forms are now recognized as separate species in the eastern slopes of the Andes. These forms are probably most closely related to cydno, but in several cases bear virtually identical colour patterns to the local race of melpomene, very likely resulting from gene transfer from that species; they therefore can and sometimes do join the local mimicry ring with melpomene and its more distantly related co-mimic Heliconius erato. I detail how recent genetic studies, together with ecological and behavioural observations, suggest that the shared colour patterns are indeed due to hybridization and transfer of mimicry adaptations between Heliconius species. These findings may have general applicability: rapidly diversifying lineages of both plants and animals may frequently share and exchange adaptive genetic variation.

Type
Chapter
Information
Speciation and Patterns of Diversity , pp. 177 - 194
Publisher: Cambridge University Press
Print publication year: 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arias, J. J. and Huertas, B. (2001) Mariposas diurnas de la Serranía de los Churumbelos, Cauca. Distribución altitudinal y diversidad de especies (Lepidoptera: Rhopalocera: Papilionoidea). Revista Colombiana de Entomologia 27, 169–176.Google Scholar
Arnold, M. L. (1997) Natural Hybridization and Evolution. Oxford University Press, Oxford.Google Scholar
Bates, H. W. (1862) Contributions to an insect fauna of the Amazon valley. Lepidoptera: Heliconidae. Transactions of the Linnean Society of London 23, 495–566.CrossRefGoogle Scholar
Beltrán, M. (1999) Evidencia genética (alozimas) para evaluar el posible orígen híbrido de Heliconius heurippa (Lepidoptera: Nymphalidae). Universidad de los Andes, Bogotá.
Beltrán, M., Jiggins, C. D., Brower, A. V. Z., Bermingham, E. and Mallet, J. (2007) Do pollen feeding and pupal-mating have a single origin in Heliconius? Inferences from multilocus sequence data. Biological Journal of the Linnean Society 92, 221–239.CrossRefGoogle Scholar
Benson, W. W. (1978) Resource partitioning in passion vine butterflies. Evolution 32, 493–518.CrossRefGoogle ScholarPubMed
Benson, W. W., Brown, K. S. and Gilbert, L. E. (1976) Coevolution of plants and herbivores: passion flower butterflies. Evolution 29, 659–680.CrossRefGoogle Scholar
Brower, A. V. Z. (1996a) A new mimetic species of Heliconius (Lepidoptera: Nymphalidae), from southeastern Colombia, revealed by cladistic analysis of mitochondrial DNA sequences. Zoological Journal of the Linnean Society 116, 317–332.CrossRefGoogle Scholar
Brower, A. V. Z. (1996b) Parallel race formation and the evolution of mimicry in Heliconius butterflies: a phylogenetic hypothesis from mitochondrial DNA sequences. Evolution 50, 195–221.CrossRefGoogle Scholar
Brown, K. S. (1981) The biology of Heliconius and related genera. Annual Review of Entomology 26, 427–456.CrossRefGoogle Scholar
Bull, V., Beltrán, M., Jiggins, C. D., et al. (2006) Polyphyly and gene flow between non-sibling Heliconius species. BMC Biology 4, 11.CrossRefGoogle ScholarPubMed
Coyne, J. A. and Orr, H. A. (2004) Speciation. Sinauer Associates, Sunderland, Mass.Google Scholar
Dasmahapatra, K. K., Silva, A., Chung, J.-W. and Mallet, J. (2007) Genetic analysis of a wild-caught hybrid between non-sister Heliconius butterfly species. Biology Letters 3, 660–663.CrossRefGoogle ScholarPubMed
Eltringham, H. (1917) On specific and mimetic relationships in the genus Heliconius. Transactions of the Entomological Society of London 1916, 101–148.Google Scholar
Emsley, M. G. (1964) The geographical distribution of the color-pattern components of Heliconius erato and Heliconius melpomene with genetical evidence for the systematic relationship between the two species. Zoologica; Scientific Contributions of the New York Zoological Society 49, 245–286.Google Scholar
Estrada, C. and Jiggins, C. D. (2002) Patterns of pollen feeding and habitat preference among Heliconius species. Ecological Entomology 27, 448–456.CrossRefGoogle Scholar
Fisher, R. A. (1930) The Genetical Theory of Natural Selection. Clarendon Press, Oxford.CrossRefGoogle Scholar
Flanagan, N. S., Tobler, A., Davison, A., et al. (2004) The historical demography of Müllerian mimicry in the neotropical Heliconius butterflies. Proceedings of the National Academy of Sciences of the United States of America 101, 9704–9709.CrossRefGoogle ScholarPubMed
Futuyma, D. J. (1998) Evolutionary Biology, 3rd edn. Sinauer, Sunderland, Mass.Google Scholar
Gilbert, L. E. (2003) Adaptive novelty through introgression in Heliconius wing patterns: evidence for a shared genetic ‘toolbox’ from synthetic hybrid zones and a theory of diversification. In: Ecology and Evolution Taking Flight: Butterflies as Model Systems (ed. Boggs, C. L.), pp. 281–318. University of Chicago Press, Chicago.Google Scholar
Giraldo, N. (2005) Posible convergencia mimética entre las especies Heliconius melpomene y H. cydno (Lepidoptera: Nymphalidae) en Florencia (Caquetá): aproximación morfológica y genética. Universidad de Los Andes, Bogotá.
Grant, P. R. (1993) Hybridization of Darwin's finches on Isla Daphne Major, Galápagos. Philosophical Transactions of the Royal Societies of London B 340, 127–139.CrossRefGoogle Scholar
Grant, B. R. and Grant, P. R. (1998) Hybridization and speciation in Darwin's finches. The role of sexual imprinting on a culturally transmitted trait. In: Endless Forms. Species and Speciation (ed. Howard, D. J.), pp. 404–422. Oxford University Press, New York.Google Scholar
Grant, P. R. and Grant, B. R. (2008) How and Why Species Multiply. The Radiation of Darwin's Finches. Princeton University Press, Princeton, NJ.Google Scholar
Jiggins, C. D., Emelianov, I. and Mallet, J. (2005) Assortative mating and speciation as pleiotropic effects of ecological adaptation: examples in moths and butterflies. In: Insect Evolutionary Ecology (ed. Fellowes, M.), pp. 451–473. Royal Entomological Society, London.Google Scholar
Jiggins, C. D., Mallarino, R., Willmott, K. R. and Bermingham, E. (2006) The phylogenetic pattern of speciation and wing pattern change in Neotropical Ithomia butterflies (Lepidoptera: Nymphalidae). Evolution 60, 1454–1466.CrossRefGoogle Scholar
Jiggins, C. D., McMillan, W. O., King, P. and Mallet, J. (1997a) The maintenance of species differences across a Heliconius hybrid zone. Heredity 79, 495–505.CrossRefGoogle Scholar
Jiggins, C. D., McMillan, W. O. and Mallet, J. L. B. (1997b) Host plant adaptation has not played a role in the recent speciation of Heliconius himera and Heliconius erato (Lepidoptera: Nymphalidae). Ecological Entomology 22, 361–365.CrossRefGoogle Scholar
Jiggins, C. D., Naisbit, R. E., Coe, R. L. and Mallet, J. (2001) Reproductive isolation caused by colour pattern mimicry. Nature 411, 302–305.CrossRefGoogle ScholarPubMed
Joron, M., Papa, R., Beltrán, M., et al. (2006) A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biology 4, e303.CrossRefGoogle Scholar
Kapan, D. D. (2001) Three-butterfly system provides a field test of Müllerian mimicry. Nature 409, 338–340.CrossRefGoogle ScholarPubMed
Kronforst, M. R., Kapan, D. D. and Gilbert, L. E. (2006a) Parallel genetic architecture of parallel adaptive radiations in mimetic Heliconius butterflies. Genetics 174, 535–539.CrossRefGoogle ScholarPubMed
Kronforst, M. R., Salazar, C., Linares, M. and Gilbert, L. E. (2007) No genomic mosaicism in a putative hybrid butterfly species. Proceedings of the Royal Society B 274, 1255–1264.CrossRefGoogle Scholar
Kronforst, M. R., Young, L. G., Blume, L. M. and Gilbert, L. E. (2006b) Multilocus analysis of admixture and introgression among hybridizing Heliconius butterflies. Evolution 60, 1254–1268.CrossRefGoogle Scholar
Kronforst, M. R., Young, L. G., Kapan, D. D., et al. (2006c) Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proceedings of the National Academy of Sciences of the United States of America 103, 6575–6580.CrossRefGoogle ScholarPubMed
Lamas, G. (1998) Comentarios taxonómicos y nomenclaturales sobre Heliconiini neotropicales, con designación de lectotipos y descripción de cuatro subespecies nuevas (Lepidoptera: Nymphalidae: Heliconiinae). Revista Peruana de Entomologia 40 (1997), 111–125.Google Scholar
Lamas, G. (2004) Heliconiinae. In: Hesperioidea – Papilionoidea (ed. Lamas, G.), pp. 261–274. Association for Tropical Lepidoptera. Scientific Publishers, Gainesville, FL.Google Scholar
Linares, M. (1989) Adaptive microevolution through hybridization and biotic destruction in the neotropics. University of Texas at Austin.
Linares, M. (1996) The genetics of the mimetic coloration in the butterfly Heliconius cydno weymeri. Journal of Heredity 87, 142–149.CrossRefGoogle Scholar
Linares, M. (1997) The ghost of mimicry past: laboratory reconstitution of an extinct butterfly ‘race’. Heredity 78, 628–635.CrossRefGoogle Scholar
Mallet, J. (1993) Speciation, raciation, and color pattern evolution in Heliconius butterflies: evidence from hybrid zones. In: Hybrid Zones and the Evolutionary Process (ed. Harrison, R. G.), pp. 226–260. Oxford University Press, New York.Google Scholar
Mallet, J. (2001a) Causes and consequences of a lack of coevolution in Müllerian mimicry. Evolutionary Ecology 13, 777–806.CrossRefGoogle Scholar
Mallet, J. (2001b) The speciation revolution. Journal of Evolutionary Biology 14, 887–888.CrossRefGoogle Scholar
Mallet, J. (2005) Hybridization as an invasion of the genome. Trends in Ecology & Evolution 20, 229–237.CrossRefGoogle ScholarPubMed
Mallet, J. (2006) What has Drosophila genetics revealed about speciation? Trends in Ecology & Evolution 21, 386–393.CrossRefGoogle Scholar
Mallet, J. (2007) Hybrid speciation. Nature (London) 446, 279–283.CrossRefGoogle ScholarPubMed
Mallet, J., Barton, N., Lamas, G., et al. (1990) Estimates of selection and gene flow from measures of cline width and linkage disequilibrium in Heliconius hybrid zones. Genetics 124, 921–936.Google ScholarPubMed
Mallet, J., Beltrán, M., Neukirchen, W. and Linares, M. (2007) Natural hybridization in heliconiine butterflies: the species boundary as a continuum. BMC Evolutionary Biology 7, 28.CrossRefGoogle ScholarPubMed
Mallet, J. and Gilbert, L. E. (1995) Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. Biological Journal of the Linnean Society 55, 159–180.Google Scholar
Mallet, J., McMillan, W. O. and Jiggins, C. D. (1998a) Estimating the mating behavior of a pair of hybridizing Heliconius species in the wild. Evolution 52, 503–510.CrossRefGoogle Scholar
Mallet, J., McMillan, W. O. and Jiggins, C. D. (1998b) Mimicry and warning color at the boundary between races and species. In: Endless Forms: Species and Speciation (ed. Howard, D. J.), pp. 390–403. Oxford University Press, New York.Google Scholar
Mavárez, J., Salazar, C., Bermingham, E., et al. (2006) Speciation by hybridization in Heliconius butterflies. Nature 441, 868–871.CrossRefGoogle ScholarPubMed
McMillan, W. O., Jiggins, C. D. and Mallet, J. (1997) What initiates speciation in passion-vine butterflies? Proceedings of the National Academy of Sciences of the United States of America 94, 8628–8633.CrossRefGoogle ScholarPubMed
Müller, F. (1879) Ituna and Thyridia; a remarkable case of mimicry in butterflies. Transactions of the Entomological Society of London 1879, xx–xxix.Google Scholar
Naisbit, R. E., Jiggins, C. D., Linares, M. and Mallet, J. (2002) Hybrid sterility, Haldane's rule, and speciation in Heliconius cydno and H. melpomene. Genetics 161, 1517–1526.Google ScholarPubMed
Naisbit, R. E., Jiggins, C. D. and Mallet, J. (2001) Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and H. melpomene. Proceedings of the Royal Society London B 268, 1849–1854.CrossRefGoogle Scholar
Naisbit, R. E., Jiggins, C. D. and Mallet, J. (2003) Mimicry: developmental genes that contribute to speciation. Evolution & Development 5, 269–280.CrossRefGoogle ScholarPubMed
Podos, J. (2001) Correlated evolution of morphology and vocal signal structure in Darwin's finches. Nature 409, 185–188.CrossRefGoogle ScholarPubMed
Salazar, C. A., Jiggins, C. D., Arias, C. F., et al. (2005) Hybrid incompatibility is consistent with a hybrid origin of Heliconius heurippa Hewitson from its close relatives, Heliconius cydno Doubleday and Heliconius melpomene Linnaeus. Journal of Evolutionary Biology 18, 247–256.CrossRefGoogle ScholarPubMed
Schluter, D. (2000) The Ecology of Adaptive Radiation. Oxford University Press, New York.Google Scholar
Seehausen, O. (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution 19, 198–207.CrossRefGoogle ScholarPubMed
Sheppard, P. M., Turner, J. R. G., Brown, K. S., Benson, W. W. and Singer, M. C. (1985) Genetics and the evolution of muellerian mimicry in Heliconius butterflies. Philosophical Transactions of the Royal Society of London B 308, 433–613.CrossRefGoogle Scholar
Turner, J. R. G. (1976) Adaptive radiation and convergence in subdivisions of the butterfly genus Heliconius (Lepidoptera: Nymphalidae). Zoological Journal of the Linnean Society 58, 297–308.CrossRefGoogle Scholar
Vane-Wright, R. I., Ackery, P. R. and Smiles, R. L. (1975) The distribution, polymorphism and mimicry of Heliconius telesiphe (Doubleday) and the species of Podotricha Michener (Lepidoptera: Heliconiinae). Transactions of the Royal Entomological Society of London 126, 611–636.CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×