Article

Nature 433, 481-487 (3 February 2005) | doi:10.1038/nature03235; Received 30 September 2004; Accepted 1 December 2004

Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila

Nicolas Gompel1,2,3, Benjamin Prud'homme1,3, Patricia J. Wittkopp1,3, Victoria A. Kassner1 & Sean B. Carroll1

  1. Howard Hughes Medical Institute and Laboratory of Molecular Biology, University of Wisconsin, 1525 Linden Drive, Madison, Wisconsin 53706, USA
  2. These authors contributed equally to this work
  3. Present addresses: Department of Zoology, Cambridge University, Downing Street, Cambridge CB2 3EJ, UK (N.G.); Department of Molecular Biology and Genetics, 227 Biotechnology Building, Cornell University, Ithaca, New York 14853, USA (P.J.W.)

Correspondence to: Sean B. Carroll1 Correspondence and requests for materials should be addressed to S.B.C. (Email: sbcarrol@wisc.edu).
The D. biarmipes y locus sequence is deposited in GenBank under accession number AY817623.

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The gain, loss or modification of morphological traits is generally associated with changes in gene regulation during development. However, the molecular bases underlying these evolutionary changes have remained elusive. Here we identify one of the molecular mechanisms that contributes to the evolutionary gain of a male-specific wing pigmentation spot in Drosophila biarmipes, a species closely related to Drosophila melanogaster. We show that the evolution of this spot involved modifications of an ancestral cis-regulatory element of the yellow pigmentation gene. This element has gained multiple binding sites for transcription factors that are deeply conserved components of the regulatory landscape controlling wing development, including the selector protein Engrailed. The evolutionary stability of components of regulatory landscapes, which can be co-opted by chance mutations in cis-regulatory elements, might explain the repeated evolution of similar morphological patterns, such as wing pigmentation patterns in flies.

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