Ancient evolutionary origin of vertebrate enteric neurons from trunk-derived neural crest.

Abstract

The enteric nervous system (ENS) of jawed vertebrates arises primarily from vagal neural crest cells that migrate to the foregut and subsequently colonize and innervate the entire gastrointestinal tract. To gain insight into its evolutionary origin, we examined ENS development in the basal jawless vertebrate, the sea lamprey. Surprisingly, we found no evidence for the existence of a vagally-derived enteric neural crest population in the lamprey. Rather, DiI labeling showed that late-migrating cells, originating from the trunk neural tube and associated with nerve fibers, differentiated into neurons within the gut wall and typhlosole. We propose that these trunk-derived neural crest cells are homologous to Schwann cell precursors (SCPs), recently shown in mammalian embryos to populate post-embryonic parasympathetic ganglia1,2, including enteric ganglia3. Our results suggest that neural crest-derived SCPs made an important contribution to the ancient ENS of early jawless vertebrates, a role that was largely subsumed by vagal neural crest cells in early gnathostomes.