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Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene

Nature volume 440, pages 1050–1053 (2006)Cite this article

Abstract

The independent evolution of morphological similarities is widespread1,2. For simple traits, such as overall body colour, repeated transitions by means of mutations in the same gene may be common3,4,5. However, for more complex traits, the possible genetic paths may be more numerous; the molecular mechanisms underlying their independent origins and the extent to which they are constrained to follow certain genetic paths are largely unknown. Here we show that a male wing pigmentation pattern involved in courtship display has been gained and lost multiple times in a Drosophila clade. Each of the cases we have analysed (two gains and two losses) involved regulatory changes at the pleiotropic pigmentation gene yellow. Losses involved the parallel inactivation of the same cis-regulatory element (CRE), with changes at a few nucleotides sufficient to account for the functional divergence of one element between two sibling species. Surprisingly, two independent gains of wing spots resulted from the co-option of distinct ancestral CREs. These results demonstrate how the functional diversification of the modular CREs of pleiotropic genes contributes to evolutionary novelty and the independent evolution of morphological similarities.

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Figure 1: Two independent gains and five losses of wing pigmentation spots in a Drosophila clade.
Figure 2: Changes in the yellow spot cis -regulatory DNA underlie the loss of the pigmentation spot in D. gunungcola.
Figure 3: A few divergent nucleotides account for the functional inactivation of the spotgun element.
Figure 4: Independent co-option of CREs of the yellow gene in wing spot evolution.

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Acknowledgements

We thank A. Kopp for sharing unpublished data; J. J. Gao, S. Hagemann, M. T. Kimura, A. Kopp, V. Stamataki and the Drosophila Tucson Stock Center for providing fly stocks; M. Toda for fly identification; M. Bate for help with behavioural observations; A. Meade and M. Pagel for advice on bayesian ancestral character reconstruction; and B. Williams and J. Yoder for comments on the manuscript. N.G. thanks P. Simpson for hosting him in her laboratory. N.G. was an EMBO and a Human Frontier long-term fellow. The project was supported by the Howard Hughes Medical Institute (S.B.C.).

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Author notes

  1. Antonis Rokas

    Present address: Broad Institute of MIT and Harvard, 320 Charles Street, Cambridge, Massachusetts, 02141-2023, USA

  2. Benjamin Prud'homme and Nicolas Gompel: *These authors contributed equally to this work

Authors and Affiliations

  1. Bock Laboratories, University of Wisconsin and Howard Hughes Medical Institute, 1525 Linden Drive, Wisconsin, 53706, Madison, USA

    Benjamin Prud'homme, Nicolas Gompel, Antonis Rokas, Victoria A. Kassner, Thomas M. Williams & Sean B. Carroll

  2. Department of Zoology, University of Cambridge, Downing Street, CB2 3EJ, Cambridge, UK

    Nicolas Gompel

  3. Department of Ecology and Evolution, Stony Brook University, 650 Life Sciences Building, New York, 11794, Stony Brook, USA

    Shu-Dan Yeh & John R. True

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Corresponding author

Correspondence to Sean B. Carroll.

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Competing interests

The sequences described in this paper have been deposited at the EMBL nucleotide database under accession numbers AM181668 to AM181680. Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Figure 1

Maximum Likelihood tree showing Bayesian Inference/Maximum Parsimony/Maximum Likelihood support value at each node. The tree includes 77 species of the melanogaster and obscura groups and two outgroup species from the willistoni group. (JPG 189 kb)

Supplementary Figure 2

D. mimetica (a) has lost its male wing spot independently from D. gunungcola, Yellow is not expressed at high levels in the putative spot region (b), as reflected by the uniform reporter expression across the wing of a wing largemim transformant (c). Specifically, the loss of Yellow expression in the prospective spot region is due to a non-functional spotmim element (d). (JPG 103 kb)

Supplementary Figure 3

Regulatory activity in the yellow intron and the origin of a spot. D. guanche adult males (a) are devoid of wing dark spot. However, the y intron from this species drives expression in the wing veins (b), as does the D. tristis y intron. In contrast, the y intron of species from the melanogaster group, such as D. biarmipes (c) does not drive spot or wing vein expression, but it does drive expression in the marginal sensory bristles of the wing. (JPG 77 kb)

Supplementary Movie 1

A sequence of courtship behaviour in Drosophila biarmipes. (MOV 4284 kb)

Supplementary Movie 2

A sequence of courtship behaviour in Drosophila tristis. (MOV 11451 kb)

Supplementary Method

Detail of the phylogenetic analysis. (DOC 75 kb)

Supplementary Table 1

Density of taxon sampling. (DOC 29 kb)

Supplementary Table 2

Number and percentage of loci and nucleotide sites per species in the data matrix. (DOC 58 kb)

Supplementary Table 3

List of primers. (DOC 52 kb)

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Prud'homme, B., Gompel, N., Rokas, A. et al. Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature 440, 1050–1053 (2006). https://doi.org/10.1038/nature04597

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