Genetic Analysis of Bristle Loss in Hybrids between Drosophila melanogaster and D. simulans Provides Evidence for Divergence of cis-Regulatory Sequences in the achaete–scute Gene Complex

Abstract

The two closely related species of Drosophila, D. melanogaster and D. simulans, display an identical bristle pattern on the notum, but hybrids between the two are lacking a variable number of bristles. We show that the loss is temperature-dependent and provide evidence for two periods of temperature sensitivity. A first period of heat sensitivity occurs during larval development and corresponds to the time when the prepattern of expression of genes whose products activate achaete–scute in the proneural clusters preceding bristle precursor formation is established. A second period of cold sensitivity corresponds to the time of emergence of the bristle precursor cells and the maintenance of their neural fate, a process requiring high levels of Achaete–Scute. Expression of achaete–scute at these two critical periods depends on cis-regulatory elements of the achaete–scute complex (AS-C). The differences between males, which have only one copy of the X-linked AS-C from D. simulans, and females, which have copies from both parental species, are compared, together with the effects of crossing in different rearrangements of the D. melanogaster AS-C that delete regulatory and/or coding sequences. We provide evidence that bristle loss in the hybrids may result from a decrease in the level of transcription at the AS-C and argue that interaction between trans-acting factors and cis-regulatory elements within the AS-C has diverged between the two species.