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Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies


Some morphological traits differ greatly between related species, but it is not clear whether diversity evolves through changes in the same genes and whether similar, independent (that is, convergent) changes occur by the same mechanism1,2. Pigmentation in fruitflies presents an attractive opportunity to explore these issues because pigmentation patterns are diverse, similar patterns have arisen in independent clades, and numerous genes governing their formation have been identified3,4,5 in Drosophila melanogaster. Here we show that both evolutionary diversification and convergence can be due to evolution at the same locus, by comparing abdominal pigmentation and trichome patterns and the expression of Bric-à-brac2 (Bab2), which regulates both traits in D. melanogaster3,6, in 13 species representing the major clades7,8 of the subfamily Drosophilinae. Modifications of Bab2 expression are frequently correlated with diverse pigmentation and trichome patterns that evolved independently in multiple lineages. In a few species, Bab2 expression is not correlated with changes in pigmentation but is correlated with a conserved pattern of trichomes, indicating that this locus can be circumvented to evolve new patterns when a correlated trait is under different constraints.

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Figure 1: Modulation of Bab2 expression is correlated with diverse abdominal pigmentation patterns.
Figure 2: Modulation of Bab2 expression underlies the diversification and evolutionary convergence of cuticular traits throughout the Drosophilinae.
Figure 3: Bab2 expression is correlated with the distribution of cuticular trichomes.

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We thank C. Nelson for help with fly collection; D. Lachaise and P. O'Grady for species identification; T. Markow, L. Andrew (Tucson Stock Center), J. Coyne and D. Lachaise for providing fly stocks; F. Laski and D. Godt for the Bab2 antibody; V. Kassner for invaluable technical assistance; A. Rokas for help with character reconstruction; and B. Williams, A. Kopp, A. Rokas and C. Nelson for discussions on the project. N.G. has been funded by the Howard Hughes Medical Institute and the Philippe foundation and is supported by an EMBO long-term post-doctoral 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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Gompel, N., Carroll, S. Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies. Nature 424, 931–935 (2003).

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