Article

Complex modular architecture around a simple toolkit of wing pattern genes

  • Nature Ecology & Evolution 1, Article number: 0052 (2017)
  • doi:10.1038/s41559-016-0052
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Abstract

Identifying the genomic changes that control morphological variation and understanding how they generate diversity is a major goal of evolutionary biology. In Heliconius butterflies, a small number of genes control the development of diverse wing colour patterns. Here, we used full-genome sequencing of individuals across the Heliconius erato radiation and closely related species to characterize genomic variation associated with wing pattern diversity. We show that variation around colour pattern genes is highly modular, with narrow genomic intervals associated with specific differences in colour and pattern. This modular architecture explains the diversity of colour patterns and provides a flexible mechanism for rapid morphological diversification.

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Acknowledgements

We thank A. Tapia for maintaining the H. erato genome line and for generating our mapping family, and M. Vargas and C. Rosales for Illumina library preparation. We acknowledge the University of Puerto Rico, the Puerto Rico INBRE grant P20 GM103475 from the National Institute for General Medical Sciences (NIGMS), a component of the National Institutes of Health (NIH); CNRS Nouraugues and CEBA awards (B.A.C.); National Science Foundation awards DEB-1257839 (B.A.C.), DEB-1257689 (W.O.M.), DEB-1027019 (W.O.M.); awards 1010094 and 1002410 from the Experimental Program to Stimulate Competitive Research (EPSCoR) program of the National Science Foundation (NSF) for computational resources; and the Smithsonian Institution. This research was supported in part by Lilly Endowment, Inc., through its support for the Indiana University Pervasive Technology Institute, and in part by the Indiana METACyt Initiative. The Indiana METACyt Initiative at IU is also supported in part by Lilly Endowment, Inc.

Author information

Author notes

    • Steven M. Van Belleghem
    •  & Pasi Rastas

    These authors contributed equally to this work.

    • Brian A. Counterman
    • , W. Owen McMillan
    •  & Riccardo Papa

    These authors jointly supervised this work.

Affiliations

  1. Department of Biology, Center for Applied Tropical Ecology and Conservation, University of Puerto Rico, Rio Piedras, Puerto Rico

    • Steven M. Van Belleghem
    • , Pasi Rastas
    • , Mayte Ruiz
    • , Brian A. Counterman
    • , W. Owen McMillan
    •  & Riccardo Papa
  2. Smithsonian Tropical Research Institute, Apartado 0843-03092, Panamá, Panama

    • Steven M. Van Belleghem
    • , Carlos F. Arias
    • , Megan A. Supple
    •  & W. Owen McMillan
  3. Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK

    • Pasi Rastas
    • , Simon H. Martin
    • , Joseph J. Hanly
    •  & Chris D. Jiggins
  4. Hawkesbury Institute for the Environment, Western Sydney University, Richmond, New South Wales 2753, Australia

    • Alexie Papanicolaou
  5. Biology Program, Faculty of Natural Sciences and Mathematics, Universidad del Rosario, Carrera. 24 No. 63C-69, Bogota, DC 111221, Colombia

    • Carlos F. Arias
    • , Camilo Salazar
    •  & Mauricio Linares
  6. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, USA

    • James Mallet
  7. Department of Ecology and Evolutionary Biology, Cornell University, 215 Tower Road, Ithaca, New York 14853-7202, USA

    • James J. Lewis
  8. Department of Biology, Pennsylvania State University, University Park, Pennsylvania 16802, USA

    • Heather M. Hines
    •  & Gilson R. P. Moreira
  9. PPG Biologia Animal, Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500, Bloco IV, Prédio 43435, Porto Alegre, RS 91501-970, Brazil

    • Brian A. Counterman
  10. Department of Biological Sciences, Mississippi State University, 295 Lee Boulevard, Mississippi 39762, USA

    • Riccardo Papa

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Contributions

S.M.V.B., B.A.C., W.O.M. and R.P. designed the study and wrote the paper. P.R., A.P. and J.J.M. conducted genome assembly. P.R. conducted linkage map and genome quality assessment. A.P. conducted genome annotation. S.M.V.B. conducted population genomic, phylogenetic and comparative genomic analyses. M.R, M.A.S, H.H. and J.J.H. conducted comparative genomic analyses. S.H.M. contributed scripts for Twisst analyses. B.A.C., W.O.M., R.P., H.H., C.D.J., J.M., M.L., C.S., C.F.A. and G.M. collected samples for sequencing.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Steven M. Van Belleghem.

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    Supplementary information

    Supplementary Figures 1–35; Supplementary Tables 1–13