Lamprey neural crest migration is Snail-dependent and occurs without a differential shift in cadherin expression

The acquisition of neural crest cells was a key step in the origin of the vertebrate body plan. An outstanding question is how neural crest cells acquired their ability to undergo an epithelial-mesenchymal transition (EMT) and migrate extensively throughout the vertebrate embryo. We tested if differential regulation of classical cadherins—a highly conserved feature of neural crest EMT and migration in jawed vertebrates—mediates these cellular behaviors in lamprey, a basal jawless vertebrate. Lamprey has single copies of the type I and type II classical cadherins (CadIA and CadIIA). CadIIA is expressed in premigratory neural crest, and requires the transcription factor Snail for proper expression, yet CadIA is never expressed in the neural tube during neural crest development, suggesting that differential regulation of classical cadherin expression is not required to initiate neural crest migration in basal vertebrates. We hypothesize that neural crest cells evolved by retention of regulatory programs linking distinct mesenchymal and multipotency properties, and emigrated from the neural tube without differentially regulating type I/type II cadherins. Our results point to the coupling of mesenchymal state and multipotency as a key event facilitating the origin of migratory neural crest cells. •Lampreys contain a single epithelial and a single mesenchymal cadherin.•A mesenchymal, but not epithelial, cadherin is expressed in lamprey neural crest.•Snail regulates mesenchymal cadherin expression in lamprey migratory neural crest.•Modulation of cadherin expression is a gnathostome novelty for neural crest migration.•Cadherin expansion in gnathostomes is likely related to evolution of a GRN migratory module.