A damped oscillator governs posterior gap gene patterning in Drosophila melanogaster

Insects use two main modes of segment determination during development: the ancestral short-
germband mode (eg. Gryllus bimaculatus), where new segments are added sequentially, and the
long-germband mode (eg. Drosophila melanogaster) where all segments are detemined
simultaneously. In dipteran insects (flies, midges and mosquitoes), where the long-germband mode
of segmentation is used, the gap genes are activated by maternal gradients and cross regulate each
other to form the first zygotic regulatory layer of the segmentation gene hierarchy. A precise
mathematical model of the gap genes in Drosophila melanogaster was obtained from quantitative
spatio-temporal expression data and used to study the dynamics of pattern formation. This approach
showed that two distinct dynamical regimes govern anterior and posterior trunk patterning.
Stationary domain boundaries in the anterior rely on bistability. In contrast, the observed anterior
shifts of posterior gap gene domains can be explained as an emergent property of an underlying
regulatory mechanism implementing a damped oscillator. We have identified a dual-function three-
gene motif embedded in the gap gene regulatory network which is sufficient to recover both
anterior and posterior dynamical regimes. Which one governs a given region depends on the gap
genes involved. This motif is known as the AC/DC circuit. The dynamical repertoire of this motif
consists of only one more possible regime, sustained oscillations, which are not found in the gap
gene system. Since molecular oscillations are characteristic of short-germband segmentation, these
findings suggest that the two modes of segment determination may have more in common than
previously thought. This insight helps us understand why long-germband segmentation may have
evolved several dozen times independently from the ancestral short-germband mode.