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Speciation by hybridization in Heliconius butterflies

An Author Correction to this article was published on 15 March 2021

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Abstract

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.

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Figure 1: Geographic distributions and genetic differentiation between H. cydno, H. melpomene and H. heurippa.
Figure 2: Reconstruction of the H. heurippa wing pattern.
Figure 3: Relative probabilities of H. heurippa males approaching and courting colour pattern models.

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References

  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)

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  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)

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  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)

    Article  PubMed  Google Scholar 

  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)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  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)

    Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

  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)

    Article  CAS  PubMed  Google Scholar 

  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)

    Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

  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)

    Google Scholar 

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

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  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)

    PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  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)

    Article  Google Scholar 

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

    Article  Google Scholar 

  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)

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

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.

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Correspondence to Jesús Mavárez or Mauricio Linares.

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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.

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

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Mavárez, J., Salazar, C., Bermingham, E. et al. Speciation by hybridization in Heliconius butterflies. Nature 441, 868–871 (2006). https://doi.org/10.1038/nature04738

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