Editors' ChoiceDevelopment

How the Fruit Fly Got His Spots

Science Signaling  27 Apr 2010:
Vol. 3, Issue 119, pp. ec127
DOI: 10.1126/scisignal.3119ec127

Theoretical analyses have suggested that the intricate patterns of a leopard’s spots or a butterfly’s wings depend on interactions between diffusible morphogens, which act locally to stimulate developmental processes, and long-range inhibitors. Werner et al. took a more concrete approach, using transgenic fruit flies to identify Wingless as the morphogen responsible for the pattern of melanin wing spots of Drosophila guttifera. D. guttifera has a characteristic pattern of wing pigmentation, with 16 black spots located on veins and 4 gray “shades” found in intervein regions. Fly wing melanin formation depends on the protein Yellow; Yellow mRNA and protein were present in pupal wings in a pattern foreshadowing that of melanin in the adult, allowing the authors to use yellow gene expression as a marker for pigmentation. Screens of flies transduced with various constructs enabled identification of a 277-bp vein spot CRE (cis-regulatory element) that drove a reporter in the pattern of the black spots and a 414-bp intervein shade CRE, which drove the intervein gray shades. When expressed in D. melanogaster, which lacks spots, the D. guttifera vein spot CRE drove reporter expression in pupal wing in a pattern resembling that of endogenous wingless. Analyses of wingless expression in D. guttifera pupae, in a closely related species, and in a D. guttifera mutant with an ectopic melanin stripe revealed a correlation between wingless expression and sites of pigment spot formation. Furthermore, in transgenic D. guttifera with ectopic wingless expression, wingless expression paralleled pigment pattern and expression of the vein spot CRE. As in wild-type flies, pigment and the vein spot CRE were present in a broader domain than that of the wingless transcript, consistent with diffusion of the Wingless morphogen. Phylogenetic analyses of pigment pattern elements, patterned wingless expression, and the vein spot CRE indicated that the complex pattern of D. guttifera pigmentation arose in a stepwise fashion. The authors conclude that a pattern of wingless expression associated with development of physical landmarks was present early in Drosophila evolution, and this was followed by evolution of a link between Wingless signaling and pigmentation. In the final stage, co-option of wingless expression at new sites yielded a complex and elaborate pattern of pigmentation superimposed on the ancestral pattern of wingless expression.

T. Werner, S. Koshikawa, T. M. Williams, S. B. Carroll, Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464, 1143–1148 (2010). [PubMed]