Speeding up anterior-posterior patterning of insects by differential initialization of the gap gene cascade

Abstract

Recently, it was shown that anterior-posterior patterning genes in the red flour beetle Tribolium castaneum are expressed sequentially in waves. However, in the fruit fly Drosophila melanogaster, an insect with a derived mode of embryogenesis compared to Tribolium, anterior-posterior patterning genes quickly and simultaneously arise as mature gene expression domains that, afterwards, undergo slight posterior-to-anterior shifts. This raises the question of how a fast and simultaneous mode of patterning, like that of Drosophila, could have evolved from a rather slow sequential mode of patterning, like that of Tribolium. In this paper, we propose a mechanism for this evolutionary transition based on a switch from a uniform to a gradient-mediated initialization of the gap gene cascade by maternal Hb. The model is supported by computational analyses and experiments.

Keywords: Clock; Clock-and-wavefront; Drosophila; Evolution; Gap genes; Gene networks; Genetic cascade; Modeling; Morphogen gradients; Patterning; Segmentation; Short-germ to long-germ evolution; Tribolium.