Letter | Published:

Speciation by hybridization in Heliconius butterflies

Naturevolume 441pages868871 (2006) | Download Citation



Speciation is generally regarded to result from the splitting of a single lineage. An alternative is hybrid speciation, considered to be extremely rare, in which two distinct lineages contribute genes to a daughter species. Here we show that a hybrid trait in an animal species can directly cause reproductive isolation. The butterfly species Heliconius heurippa is known to have an intermediate morphology and a hybrid genome1, and we have recreated its intermediate wing colour and pattern through laboratory crosses between H. melpomene, H. cydno and their F1 hybrids. We then used mate preference experiments to show that the phenotype of H. heurippa reproductively isolates it from both parental species. There is strong assortative mating between all three species, and in H. heurippa the wing pattern and colour elements derived from H. melpomene and H. cydno are both critical for mate recognition by males.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1

    Salazar, C. A. et al. Hybrid incompatibility is consistent with a hybrid origin of Heliconius heurippa Hewitson from its close relatives, Heliconius cydno Doubleday and Heliconius melpomene Linnaeus. J. Evol. Biol. 18, 247–256 (2005)

  2. 2

    Rieseberg, L. H. Hybrid origins of plant species. Annu. Rev. Ecol. Syst. 28, 359–389 (1997)

  3. 3

    Coyne, J. A. & Orr, H. A. Speciation (Sinauer, Sunderland, Massachusetts, USA, 2004)

  4. 4

    Gross, B. L. & Rieseberg, L. H. The ecological genetics of homoploid hybrid speciation. J. Hered. 96, 241–252 (2005)

  5. 5

    McCarthy, E. M., Asmussen, M. A. & Anderson, W. W. A theoretical assessment of recombinational speciation. Heredity 74, 502–509 (1995)

  6. 6

    Buerkle, C. A., Morris, R. J., Asmussen, M. A. & Rieseberg, L. H. The likelihood of homoploid hybrid speciation. Heredity 84, 441–451 (2000)

  7. 7

    Rieseberg, L. H. Crossing relationships among ancient and experimental sunflower hybrid lineages. Evolution Int. J. Org. Evolution 54, 859–865 (2000)

  8. 8

    Salzburger, W., Baric, S. & Sturmbauer, C. Speciation via introgressive hybridization in East African cichlids? Mol. Ecol. 11, 619–625 (2002)

  9. 9

    Smith, P. F., Konings, A. & Kornfield, I. Hybrid origin of a cichlid population in Lake Malawi: implications for genetic variation and species diversity. Mol. Ecol. 12, 2497–2504 (2003)

  10. 10

    Seehausen, O. Hybridization and adaptive radiation. Trends Ecol. Evol. 19, 198–207 (2004)

  11. 11

    Schwarz, D., Matta, B. M., Shakir-Botteri, N. L. & McPheron, B. A. Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436, 546–549 (2005)

  12. 12

    Brown, K. S. The biology of Heliconius and related genera. Annu. Rev. Entomol. 26, 427–456 (1981)

  13. 13

    Brown, K. S., Emmel, T. C., Eliazar, P. J. & Suomalainen, E. Evolutionary patterns in chromosome numbers in neotropical Lepidoptera. I. Chromosomes of the Heliconiini (Family Nymphalidae: Subfamily Nymphalinae). Hereditas 117, 109–125 (1992)

  14. 14

    McMillan, W. O., Jiggins, C. D. & Mallet, J. What initiates speciation in passion-vine butterflies? Proc. Natl Acad. Sci. USA 94, 8628–8633 (1997)

  15. 15

    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)

  16. 16

    Jiggins, C. D., Naisbit, R. E., Coe, R. L. & Mallet, J. Reproductive isolation caused by colour pattern mimicry. Nature 411, 302–305 (2001)

  17. 17

    Jiggins, C. D., Estrada, C. & Rodrigues, A. Mimicry and the evolution of premating isolation in Heliconius melpomene Linnaeus. J. Evol. Biol. 17, 680–691 (2004)

  18. 18

    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)

  19. 19

    Smiley, J. T. Plant chemistry and the evolution of host specificity: new evidence from Heliconius and Passiflora. Science 201, 745–747 (1978)

  20. 20

    Gilbert, L. E. in Butterflies: Ecology and Evolution Taking Flight (eds Boggs, C. L., Watt, W. B. & Ehrlich, P. R.) 281–318 (Univ. of Chicago Press, Chicago, 2003)

  21. 21

    Linares, M. Adaptive Microevolution Through Hybridization and Biotic Destruction in the Neotropics. Thesis, University of Texas, Austin (1989)

  22. 22

    Naisbit, R. E., Jiggins, C. D. & Mallet, J. Mimicry: developmental genes that contribute to speciation. Evol. Dev. 5, 269–280 (2003)

  23. 23

    Naisbit, R. E., Jiggins, C. D., Linares, M., Salazar, C. A. & Mallet, J. Hybrid sterility, Haldane's rule and speciation in Heliconius cydno and H. melpomene. Genetics 161, 1517–1526 (2002)

  24. 24

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

  25. 25

    Mallet, J. & 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)

  26. 26

    Mallet, J. Causes and consequences of a lack of coevolution in Müllerian mimicry. Evol. Ecol. 13, 777–806 (1999)

  27. 27

    Boggs, C. L. & Gilbert, L. E. Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206, 83–84 (1979)

  28. 28

    Mavárez, J. & González, M. A set of microsatellite loci for Heliconius melpomene and close relatives. Mol. Ecol. Notes 6, 20–23 (2006)

  29. 29

    Pritchard, J. K., Stephens, M. & Donnelly, P. J. Inference of population structure using multilocus genotype data. Genetics 155, 945–959 (2000)

Download references


We thank E. García and the UNET for help at Paramillo Natural Park, San Cristóbal, Venezuela; R. Castillo, L. Pereira and O. Quintero for butterfly collecting; M. Guerra and L. González for help with the preparation of figures; N. Barton and F. Jiggins for discussion; and L. Gilbert and J. Mallet for inspiring us to study hybridization. This work was funded by the Marie-Curie Fellowships, the Smithsonian Tropical Research Institute, the Fondo Colombiano de Investigaciones Científicas y Proyectos Especiales Francisco Jose de Caldas COLCIENCIAS, Banco de la República, and private donations from Continautos S.A., Proficol El Carmen S.A., Didacol S.A., and F. Arango, Colombia. C.D.J. is supported financially by the Royal Society and by a grant from BBSRC.

Author information

Author notes

  1. Jesús Mavárez and Camilo A. Salazar: *These authors contributed equally to this work


  1. Smithsonian Tropical Research Institute, Apartado postal, Panamá, 0843-03092, República de Panamá

    • Jesús Mavárez
    •  & Eldredge Bermingham
  2. Instituto de Genética, Universidad de los Andes, Santafé de D.C, Bogotá, Carrera 1E No 18ª–10, PO Box 4976, Colombia

    • Camilo A. Salazar
    • , Christian Salcedo
    •  & Mauricio Linares
  3. Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, West Mains Road, EH9 3JT, Edinburgh, UK

    • Chris D. Jiggins


  1. Search for Jesús Mavárez in:

  2. Search for Camilo A. Salazar in:

  3. Search for Eldredge Bermingham in:

  4. Search for Christian Salcedo in:

  5. Search for Chris D. Jiggins in:

  6. Search for Mauricio Linares in:

Competing interests

The sequences have been deposited in GenBank under accession numbers DQ445384–DQ445414 (Distal-less) and DQ445416–DQ445457 (Invected). Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Corresponding authors

Correspondence to Jesús Mavárez or Mauricio Linares.

Supplementary information

  1. Supplementary Notes

    This file contains Supplementary Methods, Supplementary Figures and Legends 1–8, and additional references. (PDF 681 kb)

About this article

Publication history



Issue Date



Further reading


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.