Evolution of the vertebrate New Head by progressive acquisition of neural crest regulatory subcircuits

The neural crest is a vertebrate innovation proposed to be a key component of the “New Head” that imbued vertebrates with predatory behavior. To address how evolution of this cell type impacted the vertebrate body plan, we examined the molecular circuits that control neural crest development along the anteroposterior axis of a jawless vertebrate, the sea lamprey. Gene expression analysis showed that the lamprey cranial neural crest lacks most components of an amniote cranial-specific transcriptional circuit that imbues this population with the ability to form craniofacial cartilage1. Consistent with this, hierarchical clustering revealed that the transcriptional profile of the lamprey cranial crest is more similar to the amniote trunk crest. Intriguingly, analysis of the cranial neural crest in skate and zebrafish embryos demonstrated that the cranial-specific transcriptional circuit emerged via gradual addition of network components in gnathostomes, which subsequently became restricted to the cephalic region. Our results indicate that the ancestral neural crest at the base of vertebrates possessed a trunk-like identity. We propose that the emergence of the cranial neural crest, by progressive assembly of a novel axial-specific regulatory circuit, allowed for the elaboration of the New Head during vertebrate evolution.