Abstract

The wing patterns of butterflies and moths (Lepidoptera) are diverse and striking examples of evolutionary diversification by natural selection1,2. Lepidopteran wing colour patterns are a key innovation, consisting of arrays of coloured scales. We still lack a general understanding of how these patterns are controlled and whether this control shows any commonality across the 160,000 moth and 17,000 butterfly species. Here, we use fine-scale mapping with population genomics and gene expression analyses to identify a gene, cortex, that regulates pattern switches in multiple species across the mimetic radiation in Heliconius butterflies. cortex belongs to a fast-evolving subfamily of the otherwise highly conserved fizzy family of cell-cycle regulators3, suggesting that it probably regulates pigmentation patterning by regulating scale cell development. In parallel with findings in the peppered moth (Biston betularia)4, our results suggest that this mechanism is common within Lepidoptera and that cortex has become a major target for natural selection acting on colour and pattern variation in this group of insects.

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Accessions

Primary accessions

European Nucleotide Archive

GenBank/EMBL/DDBJ

Gene Expression Omnibus

NCBI Reference Sequence

Data deposits

Short read sequence data generated for this study are available from ENA (http://www.ebi.ac.uk/ena) under study accession PRJEB8011 and PRJEB12740 (see Supplementary Table 1 for previously published data accessions). The updated Cr contig is deposited in Genbank with accession KC469893.2. The assembled H. melpomene fosmid sequences are deposited in Genbank with accessions KU514430KU514438. The microarray data are deposited in GEO with accessions GSM1563402GSM1563497.

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Acknowledgements

We thank C. Saski for assembly of the H. erato BACs; M. Abanto and A. Tapia for assistance with raising butterflies; M. Chouteau, J. Morris and K. Dasmahapatra for providing larvae for in situ hybridizations; A. Morrison, R. Tetley, S. Carl and H. Wegener for assistance with laboratory work; S. Baxter for the H. melpomene fosmid libraries; and the governments of Colombia, Ecuador, Panama and Peru for permission to collect butterflies. This work was funded by a Leverhulme Trust award (RPG-2014-167), BBSRC (H01439X/1), ERC (SpeciationGenetics 339873), and NERC small project (MGF 280) grants to C.D.J., NSF grants (DEB 1257689, IOS 1052541) to W.O.M., an ERC starting grant (StG-243179) to M.J. and French National Agency for Research (ANR) grants to M.J. (ANR-12-JSV7-0005) and V.L. (ANR-13-JSV7-0003-01). N.J.N. is funded by a NERC fellowship (NE/K008498/1).

Author information

Affiliations

  1. Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN UK

    • Nicola J. Nadeau
  2. Smithsonian Tropical Research Institute, Apartado Postal 0843-00153, Panamá, República de Panamá

    • Nicola J. Nadeau
    • , Megan A. Supple
    • , Richard W. R. Wallbank
    • , Joseph J. Hanly
    • , Richard M. Merrill
    • , W. Owen McMillan
    •  & Chris D. Jiggins
  3. Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario, Cra. 24 No 63C-69, Bogotá D.C., 111221, Colombia

    • Carolina Pardo-Diaz
    •  & Camilo Salazar
  4. Institut de Systématique, Evolution et Biodiversité (UMR 7205 CNRS, MNHN, UPMC, EPHE, Sorbonne Université), Museum National d’Histoire Naturelle, CP50, 57 rue Cuvier, 75005 Paris, France

    • Annabel Whibley
    • , Suzanne V. Saenko
    • , Violaine Llaurens
    •  & Mathieu Joron
  5. Cell and Developmental Biology, John Innes Centre, Norwich, Norfolk NR4 7UH, UK

    • Annabel Whibley
  6. Research School of Biology, The Australian National University, 134 Linnaeus Way, Acton, ACT, 2601, Australia

    • Megan A. Supple
  7. Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

    • Richard W. R. Wallbank
    • , Joseph J. Hanly
    • , Richard M. Merrill
    •  & Chris D. Jiggins
  8. Energy and Resources Group, University of California at Berkeley, California, 94720, USA

    • Grace C. Wu
  9. Department of Biology, Williams College, Williamstown, Massachusetts 01267, USA

    • Luana Maroja
  10. Department of Zoology, University of Oxford, South Parks Rd, Oxford OX1 3PS, UK

    • Laura Ferguson
  11. Penn State University, 517 Mueller, University Park, Pennsylvania 16802, USA

    • Heather Hines
  12. School of Biosciences, University of Exeter in Cornwall, Penryn, Cornwall TR10 9FE, UK

    • Andrea J. Dowling
    •  & Richard H. ffrench-Constant
  13. Centre d’Ecologie Fonctionnelle et Evolutive (CEFE, UMR 5175 CNRS, Université de Montpellier, Université Paul-Valéry Montpellier, EPHE), 1919 route de Mende, 34293 Montpellier, France

    • Mathieu Joron

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Contributions

N.J.N. performed the association analyses, 5′ RACE, RT–PCR and qRT–PCR and prepared the manuscript. N.J.N. and C.D.J. co-ordinated the research. C.P.-D. performed and analysed the microarray and RNA-seq experiments. A.W. performed the H. numata association analysis. M.A.S. assembled and annotated the HeCr BAC reference and the H. erato alignments. S.V.S. performed in situ hybridizations. R.W.R.W. performed the transgenic experiments and analysis of de novo assembled sequences and fosmids together with J.J.H. G.C.W. and L.F. initially identified splicing variants of cortex. L.M. performed crosses between H. melpomene races. H.H. screened the HeCr BAC library. C.S. and R.M.M. provided samples. A.J.D. contributed to the H. melpomene BAC sequencing and annotation. R.H.f.-C., M.J., V.L., W.O.M. and C.D.J. are PIs who obtained funding and led the project elements. All authors commented on the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Nicola J. Nadeau or Chris D. Jiggins.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Results.

  2. 2.

    Supplementary Data 1

    This file shows the alignment of fizzy family protein amino acid sequences, used to generate Extended Data Figure 6.

Excel files

  1. 1.

    Supplementary Table 1

    This file contains information on all individuals genotyped for the genotype-by-phenotype association analyses and study accessions for sequence read data.

  2. 2.

    Supplementary Table 2

    This file contains the information on all primers used.

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DOI

https://doi.org/10.1038/nature17961

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