Nervous system centralization as the evolutionary scaffold for body segmentation: A review of the evidence

Ariel D Chipman, Nitzan Alon

The evolutionary origins of two major bilaterian innovations, the centralized nervous system and the segmented body plan, have both been debated as cases of homology versus convergence, often using strikingly similar arguments. Here we review the comparative developmental genetics of both processes across the three segmented animal phyla (arthropods, annelids, and chordates) focusing on the overlapping toolkit used in both: Notch/Delta signaling, the segment-polarity gene engrailed, Wnt signaling, and the transcription factors Krüppel and hunchback. We show that each carries dual roles in neural specification and in segmentation, and that in several cases the neural function appears to be evolutionarily ancestral. We argue that the shared architecture of the motor unit, which couples segmentally reiterated neurons to their muscle targets, provides the mechanistic link that allowed neural patterning networks to be repeatedly co-opted for trunk segmentation. This scenario supports a "brain-first" hypothesis, in which nervous system centralization arose before, and served as the developmental scaffold for, segmented body plans. We conclude that segmentation is likely not a homologous character, but a convergent elaboration built repeatedly from a shared, ancestral neural toolkit, through the co-option of conserved neurogenic gene regulatory networks.