Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

Journal name:
Nature
Volume:
487,
Pages:
94–98
Date published:
DOI:
doi:10.1038/nature11041
Received
Accepted
Published online

The evolutionary importance of hybridization and introgression has long been debated1. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation2, 3, 4, 5. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

At a glance

Figures

  1. Distribution, mimicry and phylogenetic relationships of sequenced taxa.
    Figure 1: Distribution, mimicry and phylogenetic relationships of sequenced taxa.

    a, Phylogenetic relationship of sequenced species and subspecies in the melpomene–silvaniform clade of Heliconius. Heliconius elevatus falls in the silvaniform clade, but it mimics colour patterns of melpomenetimareta clade taxa. Most other silvaniforms mimic unrelated ithomiine butterflies24. b, Geographic distribution of postman and rayed H.melpomene races studied here (blue, yellow and purple), and the entire distribution of H.melpomene (grey). The H.timareta races investigated have limited distributions (red) indicated by arrows and mimic sympatric races of H.melpomene. Heliconius elevatus and the other silvaniform species are distributed widely across the Amazon basin (Supplementary Information, section 22).

  2. Comparative analysis of synteny and expansion of the chemosensory genes.
    Figure 2: Comparative analysis of synteny and expansion of the chemosensory genes.

    a, Maps of the 21 Heliconius chromosomes (colour) and of the 28 Bombyx chromosomes (grey) based on positions of 6,010 orthologue pairs demonstrate highly conserved synteny and a shared n = 31 ancestor (Supplementary Information, section 8). Dotted lines within chromosomes indicate major chromosomal fusions. b, Maximum-likelihood tree showing expansions of chemosensory protein (CSP) genes in the two butterfly genomes.

  3. Four-taxon ABBA/BABA test of introgression.
    Figure 3: Four-taxon ABBA/BABA test of introgression.

    a, ABBA and BABA nucleotide sites employed in the test are derived (–B–) in H.timareta compared with the silvaniform outgroup (–A), but differ among H.melpomene amaryllis and H.melpomene aglaope (either ABBA or BABA). As this almost exclusively restricts attention to sites polymorphic in the ancestor of H.timareta and H.melpomene, equal numbers of ABBA and BABA sites are expected under a null hypothesis of no introgression22, as depicted in the two gene genealogies. b, Distribution among chromosomes of Patterson’s D-statistic (±s.e.), which measures excess of ABBA sites over BABA sites22, here for the comparison: H.m.aglaope, H.m.amaryllis, H.timareta ssp. nov., silvaniform. Chromosomes containing the two colour-pattern regions (B/D, red; N/Yb, yellow) have the two highest D-statistics; the combinatorial probability of this occurring by chance is 0.005. The excess of ABBA sites (0<D<1) indicates introgression between sympatric H.timareta and H.m.amaryllis.

  4. Evidence for adaptive introgression at the B/D mimicry locus.
    Figure 4: Evidence for adaptive introgression at the B/D mimicry locus.

    a, Genetic divergence between H.melpomene races aglaope (rayed) and amaryllis (postman) across a hybrid zone in northeast Peru. Divergence, FST, is measured along the B/D region (Supplementary Information 14) and peaks in the region known to control red wing pattern elements between the genes kinesin and optix23. b, c, Distribution of fixed ABBA and BABA sites (see Fig. 3a) along B/D for two comparisons. Excesses of ABBA in b and BABA in c are highly significant (two-tailed Z-tests for D = 0; D = 0.90±0.13, P = 5×10−14 and D = −0.91±0.10, P = 9×10−24, respectively), indicating introgression. d, e, f, Genealogical change along B/D investigated with maximum likelihood based on 50-kb windows. Three representative tree topologies are shown. Topology A, the species tree, is found within the white windows. In topologies B (dark green window) and C (light green windows) taxa group by colour pattern rather than by species. Within striped windows, H.melpomene and/or H.timareta are paraphyletic but the taxa do not group by colour pattern. Support is shown for nodes with >50% bootstrap support (Supplementary Information, section 19). bp, base pair.

References

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Author information

Affiliations

  1. Department of Genetics, Evolution and Environment, University College London, Gower Street, London WC1E 6BT, UK.

    • Kanchon K. Dasmahapatra,
    • Neil Rosser &
    • James Mallet
  2. Department of Zoology, Downing Street, University of Cambridge, Cambridge CB2 3EJ, UK.

    • James R. Walters,
    • Nicola J. Nadeau,
    • Simon H. Martin,
    • Camilo Salazar,
    • Simon W. Baxter,
    • Alison Surridge &
    • Chris D. Jiggins
  3. Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697, USA.

    • Adriana D. Briscoe,
    • James J. Lewis,
    • Arnaud Martin,
    • Furong Yuan &
    • Robert D. Reed
  4. Institute of Evolutionary Biology, Ashworth Laboratories, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK.

    • John W. Davey &
    • Mark L. Blaxter
  5. CNRS UMR 7205, Muséum National d’Histoire Naturelle, 45 rue Buffon, Paris 75005, France.

    • Annabel Whibley,
    • Robert T. Jones &
    • Mathieu Joron
  6. Institute for Physical Science and Technology, University of Maryland, College Park, Maryland 20742, USA.

    • Aleksey V. Zimin &
    • James A. Yorke
  7. European Bioinformatics Institute, Hinxton CB10 1SD, UK.

    • Daniel S. T. Hughes,
    • Paul Kersey,
    • Daniel Lawson &
    • Derek Wilson
  8. Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.

    • Laura C. Ferguson &
    • Peter W. H. Holland
  9. Smithsonian Tropical Research Institute, Smithsonian Tropical Research Institute, Apartado Postal 0843-03092, Panamá, República de Panamá.

    • Camilo Salazar,
    • W. Owen McMillan &
    • Chris D. Jiggins
  10. Institut für Mathematik und Informatik, Universität Greifswald, 17487 Greifswald, Germany.

    • Sebastian Adler &
    • Katharina J. Hoff
  11. Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.

    • Seung-Joon Ahn,
    • David G. Heckel,
    • Yannick Pauchet &
    • Heiko Vogel
  12. Ecology and Evolution, Imperial College London, London SW7 2AZ, UK.

    • Dean A. Baker
  13. FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.

    • Nicola L. Chamberlain,
    • Ayse Tenger-Trolander &
    • Marcus R. Kronforst
  14. Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Penryn TR10 9EZ, UK.

    • Ritika Chauhan &
    • Richard H. ffrench-Constant
  15. Department of Biology, Mississippi State University, Mississippi State, Mississippi 39762, USA.

    • Brian A. Counterman
  16. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK.

    • Tamas Dalmay
  17. Section of Integrative Biology and Brackenridge Field Laboratory, University of Texas, Austin, Texas 78712, USA.

    • Lawrence E. Gilbert
  18. Black Mountain Laboratories, CSIRO Ecosystem Sciences, Clunies Ross Street, Canberra, Australian Capital Territory 2601, Australia.

    • Karl Gordon &
    • Alexie Papanicolaou
  19. Department of Genetics, North Carolina State University, Raleigh, North Carolina 27695, USA.

    • Heather M. Hines
  20. UMR-A 1272 INRA-Université Pierre et Marie Curie, Physiologie de l’Insecte: Signalisation et Communication, Route de Saint-Cyr, Versailles Cedex 78026, France.

    • Emmanuelle Jacquin-Joly
  21. Department of Genetics, Downing Street, University of Cambridge, Cambridge CB2 3EH, UK.

    • Francis M. Jiggins &
    • William J. Palmer
  22. Department of Entomology, Center for Comparative Genomics, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, California 94118, USA.

    • Durrell D. Kapan
  23. Center for Conservation and Research Training, Pacific Biosciences Research Center, University of Hawaii at Manoa, 3050 Maile Way, Gilmore 406, Honolulu, Hawaii 96822, USA.

    • Durrell D. Kapan
  24. Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Apartado 14-0434, Lima, Peru.

    • Gerardo Lamas
  25. School of Computing Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK.

    • Daniel Mapleson
  26. Department of Biology, Williams College, Williamstown, Massachusetts 01267, USA.

    • Luana S. Maroja
  27. Department of Genetics, Yale University School of Medicine, 333 Cedar Street, New Haven, Connecticut 06520, USA.

    • Simon Moxon
  28. Department of Biology, University of Puerto Rico, PO Box 23360, Río Piedras, 00931-3360 Puerto Rico.

    • Riccardo Papa
  29. Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, Mississippi 39762, USA.

    • David A. Ray
  30. Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, Mississippi 39759, USA.

    • David A. Ray
  31. McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, Baltimore, Maryland 21205, USA.

    • Steven L. Salzberg
  32. Biomathematics Program, North Carolina State University, Raleigh, North Carolina 27695, USA.

    • Megan A. Supple
  33. School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK.

    • Paul A. Wilkinson
  34. The GenePool, Ashworth Laboratories, University of Edinburgh, West Mains Road, Edinburgh EH9 3JT, UK.

    • Alexi L. Balmuth,
    • Cathlene Eland,
    • Karim Gharbi,
    • Marian Thomson &
    • Mark L. Blaxter
  35. Human Genome Sequencing Center, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030, USA.

    • Richard A. Gibbs,
    • Yi Han,
    • Joy C. Jayaseelan,
    • Christie Kovar,
    • Tittu Mathew,
    • Donna M. Muzny,
    • Fiona Ongeri,
    • Ling-Ling Pu,
    • Jiaxin Qu,
    • Rebecca L. Thornton,
    • Kim C. Worley,
    • Yuan-Qing Wu,
    • Steven E. Scherer &
    • Stephen Richards
  36. Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario and Instituto de Genética, Universidad de los Andes, Bogotá, Colombia.

    • Mauricio Linares
  37. Department of Biology, Boston University, 5 Cummington Street, Boston, Massachusetts 02215, USA.

    • Sean P. Mullen
  38. Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138, USA.

    • James Mallet

Consortia

  1. The Heliconius Genome Consortium

    • Kanchon K. Dasmahapatra,
    • James R. Walters,
    • Adriana D. Briscoe,
    • John W. Davey,
    • Annabel Whibley,
    • Nicola J. Nadeau,
    • Aleksey V. Zimin,
    • Daniel S. T. Hughes,
    • Laura C. Ferguson,
    • Simon H. Martin,
    • Camilo Salazar,
    • James J. Lewis,
    • Sebastian Adler,
    • Seung-Joon Ahn,
    • Dean A. Baker,
    • Simon W. Baxter,
    • Nicola L. Chamberlain,
    • Ritika Chauhan,
    • Brian A. Counterman,
    • Tamas Dalmay,
    • Lawrence E. Gilbert,
    • Karl Gordon,
    • David G. Heckel,
    • Heather M. Hines,
    • Katharina J. Hoff,
    • Peter W. H. Holland,
    • Emmanuelle Jacquin-Joly,
    • Francis M. Jiggins,
    • Robert T. Jones,
    • Durrell D. Kapan,
    • Paul Kersey,
    • Gerardo Lamas,
    • Daniel Lawson,
    • Daniel Mapleson,
    • Luana S. Maroja,
    • Arnaud Martin,
    • Simon Moxon,
    • William J. Palmer,
    • Riccardo Papa,
    • Alexie Papanicolaou,
    • Yannick Pauchet,
    • David A. Ray,
    • Neil Rosser,
    • Steven L. Salzberg,
    • Megan A. Supple,
    • Alison Surridge,
    • Ayse Tenger-Trolander,
    • Heiko Vogel,
    • Paul A. Wilkinson,
    • Derek Wilson,
    • James A. Yorke,
    • Furong Yuan,
    • Alexi L. Balmuth,
    • Cathlene Eland,
    • Karim Gharbi,
    • Marian Thomson,
    • Richard A. Gibbs,
    • Yi Han,
    • Joy C. Jayaseelan,
    • Christie Kovar,
    • Tittu Mathew,
    • Donna M. Muzny,
    • Fiona Ongeri,
    • Ling-Ling Pu,
    • Jiaxin Qu,
    • Rebecca L. Thornton,
    • Kim C. Worley,
    • Yuan-Qing Wu,
    • Mauricio Linares,
    • Mark L. Blaxter,
    • Richard H. ffrench-Constant,
    • Mathieu Joron,
    • Marcus R. Kronforst,
    • Sean P. Mullen,
    • Robert D. Reed,
    • Steven E. Scherer,
    • Stephen Richards,
    • James Mallet,
    • W. Owen McMillan &
    • Chris D. Jiggins

Contributions

Consortium leaders: C.D.J., W.O.M. Heliconius Genome Consortium Principal Investigators: R.H.f.-C., M.R.K., M.J., J.M., S.M., R.D.R, M.L.B., L.E.G., M.L., G.L. Introgression study leader: J.M. Lead investigators: K.K.D., J.R.W., N.J.N., A.W., J.W.D., A.D.B., L.C.F., D.S.T.H., S.M., C.S., J.J.L., A.V.Z. Sequencing: S.R., S.E.S., A.L.B., M.T., K.Gharbi, C.E., M.L.B., R.A.G., Y.H., J.C.J., C.K., T.M., D.M.M., F.O., L.-L.P., J.Q., R.L.T., K.C.W., Y.-Q.W. Assembly: A.V.Z., J.A.Y., S.L.S., A.P., K.Gordon. RAD map and assembly verification: J.W.D., S.W.B., M.L.B., L.S.M., D.D.K., J.R.W., P.A.W. Geographic distribution map: N.R. Annotation: J.R.W., D.S.T.H., D.W., D.L., K.J.H., S.A., P.A.W., P.K. Genome browser and databases: D.S.T.H., J.J.L. Manual annotation and evolutionary analyses: A.D.B., E.J.-J., F.Y. (olfactory proteins); L.C.F., P.W.H.H., J.R.W. (Hox genes); A.S., T.D., D.M., S.M. (microRNAs); W.J.P., F.M.J. (immune genes); R.T.J., R.C. (P450 genes); H.V., S.-J.A., D.G.H. (uridine diphosphate glucuronosyltransferase genes); Y.P. (ribosomal proteins); S.W.B., M.L.B., A.D.B., N.L.C., B.A.C., L.C.F., H.M.H., C.D.J., F.M.J., M.J., D.D.K., M.R.K., J.M., A.M., S.P.M., N.J.N., W.J.P, R.P., M.A.S., A.T.-T., A.W., F.Y. (manual annotation group); B.A.C., D.A.R. (transposable elements); D.A.B. (orthologue predictions); A.W., J.W.D., D.G.H., K. Gordon (synteny); K.K.D., N.J.N., J.W.D., S.H.M., C.S., C.D.J., M.J., J.M. (introgression analysis). K.K.D. and J.R.W. contributed equally to this work.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

The genome sequence has been submitted to the European Nucleotide Archive under accession numbers HE667773–HE672081. Additional short read sequences have been submitted to the European Nucleotide Archive under accession numbers ERP000993 and ERP000991.

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    Supplementary information

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