Article

The genetics of monarch butterfly migration and warning colouration

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Abstract

The monarch butterfly, Danaus plexippus, is famous for its spectacular annual migration across North America, recent worldwide dispersal, and orange warning colouration. Despite decades of study and broad public interest, we know little about the genetic basis of these hallmark traits. Here we uncover the history of the monarch’s evolutionary origin and global dispersal, characterize the genes and pathways associated with migratory behaviour, and identify the discrete genetic basis of warning colouration by sequencing 101 Danaus genomes from around the globe. The results rewrite our understanding of this classic system, showing that D. plexippus was ancestrally migratory and dispersed out of North America to occupy its broad distribution. We find the strongest signatures of selection associated with migration centre on flight muscle function, resulting in greater flight efficiency among migratory monarchs, and that variation in monarch warning colouration is controlled by a single myosin gene not previously implicated in insect pigmentation.

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Accessions

Primary accessions

Sequence Read Archive

Data deposits

Sequence data are deposited in the NCBI Short Read Archive (SRA) database (accession numbers SRP045457 and SRP045468).

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Acknowledgements

We thank B. Ballister, S. Barribeau, R. Bartel, N. Chamberlain, R. Cook, A. Davis, D. Feary, D. Frey, M. Maudsley, G. Moreira, E. Osburn, R. Rarick, E. Rendon, D. Rodrigues, E. Sternberg and J. Stimson for assistance collecting or providing specimens. We also thank J. Jensen and D. Lohman for discussion. This work was supported by National Institutes of Health grant GM086794-02S1, National Science Foundation grants IOS-134367, DEB-0643831, DEB-1019746 and DEB-1316037, start-up funds from the Chinese Academy of Sciences and Shanghai Institutes for Biological Sciences, and Neubauer Funds from the University of Chicago.

Author information

Affiliations

  1. Key Laboratory of Insect Developmental and Evolutionary Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China

    • Shuai Zhan
  2. Department of Ecology & Evolution, University of Chicago, Chicago, Illinois 60637, USA

    • Shuai Zhan
    • , Wei Zhang
    •  & Marcus R. Kronforst
  3. Department of Neurobiology, University of Massachusetts Medical School, Worcester, Massachusetts 01605, USA

    • Shuai Zhan
    •  & Steven M. Reppert
  4. Department of Biology, Stanford University, Stanford, California 94305, USA

    • Kristjan Niitepõld
    •  & Jeremy Hsu
  5. Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland

    • Kristjan Niitepõld
  6. Departamento de Botánica, Ecología y Fisiología Vegetal, Universidad de Córdoba, 14071 Córdoba, Spain

    • Juan Fernández Haeger
  7. School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia

    • Myron P. Zalucki
  8. Odum School of Ecology, University of Georgia, Athens, Georgia 30602, USA

    • Sonia Altizer
  9. Department of Biology, Emory University, Atlanta, Georgia 30322, USA

    • Jacobus C. de Roode

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Contributions

S.Z. designed and implemented analyses of dispersal and migration and co-wrote the manuscript. W.Z. performed wing colour analyses. K.N. performed respirometry experiments. J.H. helped design the project and collected and prepared samples for sequencing. J.F.H. and M.P.Z. provided samples and interpreted results. S.A., J.C.d.R. and S.M.R. helped design the project, provided samples, and interpreted results. M.R.K. conceived and directed the project, performed targeted population genetic analyses, and co-wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Shuai Zhan or Marcus R. Kronforst.

Extended data

Supplementary information

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    Supplementary Information

    This file contains Supplementary Tables 1-14.

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