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Generation of a novel wing colour pattern by the Wingless morphogen

Abstract

The complex, geometric colour patterns of many animal bodies have important roles in behaviour and ecology. The generation of certain patterns has been the subject of considerable theoretical exploration, however, very little is known about the actual mechanisms underlying colour pattern formation or evolution. Here we have investigated the generation and evolution of the complex, spotted wing pattern of Drosophila guttifera. We show that wing spots are induced by the Wingless morphogen, which is expressed at many discrete sites that are specified by pre-existing positional information that governs the development of wing structures. Furthermore, we demonstrate that the elaborate spot pattern evolved from simpler schemes by co-option of Wingless expression at new sites. This example of a complex design developing and evolving by the layering of new patterns on pre-patterns is likely to be a general theme in other animals.

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Figure 1: The D. guttifera wing exhibits a complex pigmentation pattern.
Figure 2: Two yellow CREs encode the elaborate D. guttifera pattern.
Figure 3: The pattern of wingless expression foreshadows the adult wing spot pattern.
Figure 4: Wingless is sufficient to induce wing pigmentation.
Figure 5: Co-option of wingless expression and the origin of a complex colour pattern.

Accession codes

Data deposits

Gene sequences from D. guttifera and D. deflecta have been deposited at GenBank under accession numbers GU591398–GU591403.

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Acknowledgements

We thank S. Blair and E. Bier for suggesting Wingless as a candidate inducer; E. Wimmer for the piggyBac, mariner, Hermes and Minos transposon vectors; E. Hare and M. Eisen for the D. guttifera genomic library; M. Rebeiz, K. Vaccaro, V. Kassner, J. Selegue and B. Prud’homme for technical advice; A. Martinez-Arias for discussions; J. Jaenike for D. nigromaculata flies; H. Krause and L. Baev for the UAS-wg construct; B. Prud’homme, H. Dufour, M. Rebeiz, H. Chung and T. Shirangi for comments on the manuscript; and L. Olds for help with the artwork. This work was supported by a Human Frontiers Science Program Fellowship (LT00640/2005-L) to T.W., a JSPS Postdoctoral Fellowship for Research Abroad to S.K., a National Institutes of Health Postdoctoral fellowship (GM076935) to T.M.W., and the Howard Hughes Medical Institute (S.B.C.).

Author Contributions T.W. and S.K. contributed equally to the experimental work. T.M.W. identified crossvein CREs from several species. T.W., S.K. and S.B.C wrote and prepared the manuscript for publication.

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Correspondence to Sean B. Carroll.

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Werner, T., Koshikawa, S., Williams, T. et al. Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464, 1143–1148 (2010). https://doi.org/10.1038/nature08896

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