Evolution of segmentation and expression domains in body plan patterning

Bateson's 1894 catalogue of variation indexed changes in the number of segments in arthropods, alongside homoeosis in appendages and axial duplicity¹. Morgan (1901) described how annelids regenerate. In regeneration from the posterior end of a piece of an earthworm, new segments form just in front of the terminal segment, and the youngest lies next to it. The process continues until the full complement is made up². Rádl (1930) summarised the classification of the evolutionary morphologists. In that classification, differentiated segmentation in insects is a higher stage than the simple repetition seen in annelids⁵.

Child (1921) noted that annelids, arthropods and all vertebrates are made of segments. He called the origin of segmentation a great problem of speculative morphology³. He contrasted two conceptions of the segment. In one, segmentation is a modified form of agamic reproduction, and each segment is a zooid that is integrated into the whole. Child objected that the theories had been morphological rather than physiological. He also found the mesodermal theory hard to defend on physiological grounds⁴.

In Drosophila, maternal gradients set the polarity of the embryo. The gap genes hunchback, Krüppel, knirps and giant are among their earliest targets. They are expressed in broad, overlapping domains⁶. Manu and colleagues (2009) measured domain borders against the Bicoid gradient. The Bicoid threshold position varied with a standard deviation of 4.6% egg length.

Ten Tusscher and Hogeweg (2011) tested an idea that had been repeatedly argued. The idea was that modularity of gene regulatory networks is key to increased body plan complexity⁸. They ran simulations that selected independently for segmentation and differentiation, which they describe as major innovations in metazoan evolution. They ran 50 simulations. They analysed whether segments and domains evolved sequentially or together, and what network architecture and dynamics resulted⁸. They report two distinct evolutionary strategies.