Those who are intimate with the fruitfly Drosophila melanogaster will recognize this fine specimen as a male. Most notably, the last two of its abdominal segments are pigmented. The equivalent segments in the posterior abdomen of females lack pigment, and sexual dimorphism of this and many other forms is responsible for all sorts of male–female behavioural differences in all sorts of organisms — vertebrate and invertebrate. Thomas Williams and colleagues have dissected this instance of fruitfly sexual dimorphism in molecular detail to reveal the genetic switch concerned (T. M. Williams et al. Cell 134, 610–623; 2008).

The pigmentation is regulated by the tandem duplicate bab genes, whose protein products repress the enzyme system that produces pigment. The authors' investigations centred on their discovery of two cis-regulatory elements that respectively control bab expression in the anterior and posterior segments, these elements being themselves binding sites for transcription factors. One of the transcription factors is ABD-B, a member of the famed HOX family; two others are forms of the Doublesex protein, one specific for males, the other for females.

Credit: BLICKWINKEL/ALAMY

The sex-specific differences in the posterior segments arise from different control of the cis-regulatory element. In females, a combination of the transcription factors ABD-B and the female-specific form of Doublesex activates bab expression (and so prevents pigmentation). In males, the male-specific form of Doublesex overrides the activating effect of ABD-B: bab is repressed, so unleashing the enzyme system that pigments the final two male segments.

The most intricate part of the authors' work, however, comes in their studies of the evolution of this switch. From comparisons with transcription-factor binding sites on the equivalent cis-regulatory element of another species of Drosophila, D. willistoni, they aimed to identify the molecular changes that occurred in the lineage of D. melanogaster arising from a putative monomorphic common ancestor. The authors' conclusion is that rather than a wholesale gain of ABD-B or Doublesex binding sites, the advent of male pigmentation was due to a suite of fine-scale changes in the number, polarity and topology of sites.

Williams et al. don't go into the possible evolutionary and ecological factors that drove the production of male pigmentation. Instead, they end with the thought that, in evolutionary history, some of the main differences in the body plans of arthropods, like Drosophila, and vertebrates have arisen from alterations in the pattern of gene expression along the principal body axis. Their work, they say, shows a general way in which such expression patterns could evolve through the accumulation of many fine-scale alterations to a gene's cis-regulatory elements.