Abstract
The distribution of sensory bristles on the thorax of Diptera (true flies) provides a useful model for the study of the evolution of spatial patterns. Large bristles called macrochaetes are arranged into species-specific stereotypical patterns determined via spatially discrete expression of the proneural genes achaete–scute (ac–sc). In Drosophila ac-sc expression is regulated by transcriptional activation at sites where bristle precursors develop and by repression outside of these sites. Three genes, extramacrochaetae (emc), hairy (h) and stripe (sr), involved in repression have been documented. Here we demonstrate that in Drosophila, the repressor genes emc and h, like sr, play an essential role in the development of structures forming part of the flight apparatus. In addition we find that, in Calliphora vicina a species diverged from D. melanogaster by about 100Myr, spatial expression of emc, h and sr is conserved at the location of development of those structures. Based on these findings we argue, first, that the role emc, h and sr in development of the flight apparatus preceded their activities for macrochaete patterning; second, that species-specific variation in activation and repression of ac-sc expression is evolving in parallel to establish a unique distribution of macrochaetes in each species.
Highlights
Modification of their regulatory capacity, variation in cis-regulatory element composition at gene targets or changes in protein interaction domains in target proteins (Averof and Akam, 1995; Averof and Patel, 1997; Sucena and Stern, 2000; Alonso et al, 2001; Ronshaugen et al, 2002; Gompel et al, 2005; Erwin and Davidson, 2009)
Activation requires numerous cis-acting regulatory elements scattered throughout the ac-sc complex (AS-C) that appear to have evolved along with duplication events at the AS-C in the lineage leading to the Cyclorrapha (Gomez-Skarmeta et al, 1995; Skaer et al, 2002; Negre and Simpson, 2009)
Are all three genes required for the development of these structures? The flight motor of the Diptera is a highly conserved feature that was probably present in an early ancestor of this insect order long before macrochaetes appeared
Summary
Modification of their regulatory capacity, variation in cis-regulatory element composition at gene targets or changes in protein interaction domains in target proteins (Averof and Akam, 1995; Averof and Patel, 1997; Sucena and Stern, 2000; Alonso et al, 2001; Ronshaugen et al, 2002; Gompel et al, 2005; Erwin and Davidson, 2009). Three antagonists have been studied, the products of the genes stripe (sr), extramacrochaetae (emc) and hairy (h) They are expressed in partially overlapping discrete spatial domains and are sufficient to correctly position bristle precursors under experimental conditions of uniform Sc expression (Rodriguez et al, 1990; Cubas and Modolell, 1992; Brand et al, 1993; Dominguez and Campuzano, 1993; Fernandes et al, 1996; Usui et al, 2008). Patterning of bristles by emc, h and sr would not require the evolution of any new features at the AS-C itself, whereas patterning through transcriptional activation is associated with gene duplication and the acquisition of numerous cis-regulatory elements (Skaer et al, 2002; Simpson and Marcellini, 2006; Negre and Simpson, 2009). We argue that the two mechanisms might have evolved sequentially
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