Evidence for the temporal regulation of insect segmentation by a conserved sequence of transcription factors

Abstract

Long-germ insects, such as the fruit fly <i>Drosophila melanogaster</i>, pattern their segments simultaneously, whereas short-germ insects, such as the beetle <i>Tribolium castaneum</i>, pattern their segments sequentially, from anterior to posterior. While the two modes of segmentation at first appear quite distinct, much of this difference might simply reflect developmental heterochrony. We now show here that, in both <i>Drosophila</i> and <i>Tribolium</i>, segment patterning occurs within a common framework of sequential Caudal, Dichaete, and Odd-paired expression. In <i>Drosophila</i> these transcription factors are expressed like simple timers within the blastoderm, while in <i>Tribolium</i> they form wavefronts that sweep from anterior to posterior across the germband. In <i>Drosophila</i>, all three are known to regulate pair-rule gene expression and influence the temporal progression of segmentation. We propose that these regulatory roles are conserved in short-germ embryos, and that therefore the changing expression profiles of these genes across insects provide a mechanistic explanation for observed differences in the timing of segmentation. In support of this hypothesis we demonstrate that Odd-paired is essential for segmentation in <i>Tribolium</i>, contrary to previous reports.