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

Abstract

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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Figure 1: Expression of the Yellow protein prefigures adult wing pigmentation.
Figure 2: Cis-regulatory changes at the yellow locus are responsible for species-specific differences in Yellow distribution.
Figure 3: The cis-regulatory sequences governing spot formation evolved in the context of an ancestral wing enhancer.
Figure 4: The spot element evolved through the acquisition of sites for both activators and repressors.
Figure 5: Concerted changes in the expression of Yellow and Ebony underlie the evolution of novel wing patterns.
Figure 6: Cryptic prepatterns and the evolution of novel gene expression patterns through the evolution of cis-regulatory sequences.

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Acknowledgements

We thank J. True, C. E. Nelson, C. M. Walsh and C. T. Hittinger for technical advice; J. True, S. Blair and members of the Carroll laboratory for discussions; B. L. Williams and J. Yoder for critical comments on the manuscript; S. Castrezana and T. Markow (Tucson Drosophila Stock Center) for providing Drosophila stocks; J. P. Gruber for the Euxesta sample; and S. Barolo for the pH Stinger vector. N.G. was funded by an EMBO long-term postdoctoral fellowship; B.P. and N.G. are recipients of a Philippe Foundation fellowship. The project was supported by the Howard Hughes Medical Institute (S.B.C.).

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Correspondence to Sean B. Carroll.

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Supplementary information

Supplementary Figure 1

Sequence alignment of the wing enhancers of D. melanogaster, D. biarmipes and D. pseudoobscura. (DOC 44 kb)

Supplementary Table 1

Sequences of oligonucleotides used for reporter constructs. (DOC 30 kb)

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Gompel, N., Prud'homme, B., Wittkopp, P. et al. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433, 481–487 (2005). https://doi.org/10.1038/nature03235

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