1. University of Wisconsin and Howard Hughes Medical Institute, Bock Laboratories, 1525 Linden Drive, Madison, Wisconsin 53706, USA
2. Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
3. Department of Ecology and Evolution, 650 Life Sciences Building, Stony Brook University, Stony Brook, New York 11794, USA
4. †Present address: Broad Institute of MIT and Harvard, 320 Charles Street, Cambridge, Massachusetts 02141-2023, USA
5. *These authors contributed equally to this work

Correspondence to: Sean B. Carroll¹ Correspondence and requests for materials should be addressed to S.B.C. (Email: sbcarrol@wisc.edu). The sequences described in this paper have been deposited at the EMBL nucleotide database under accession numbers AM181668 to AM181680.

Abstract

The independent evolution of morphological similarities is widespread^{1, 2}. For simple traits, such as overall body colour, repeated transitions by means of mutations in the same gene may be common^{3, 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.

1. University of Wisconsin and Howard Hughes Medical Institute, Bock Laboratories, 1525 Linden Drive, Madison, Wisconsin 53706, USA
2. Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK
3. Department of Ecology and Evolution, 650 Life Sciences Building, Stony Brook University, Stony Brook, New York 11794, USA
4. †Present address: Broad Institute of MIT and Harvard, 320 Charles Street, Cambridge, Massachusetts 02141-2023, USA
5. *These authors contributed equally to this work

Correspondence to: Sean B. Carroll¹ Correspondence and requests for materials should be addressed to S.B.C. (Email: sbcarrol@wisc.edu). The sequences described in this paper have been deposited at the EMBL nucleotide database under accession numbers AM181668 to AM181680.

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