Progressive acquisition of novel neural crest derivatives along the neural axis during vertebrate evolution

The neural crest is a uniquely vertebrate cell type that is thought to have played an important
role in vertebrate evolution by forming peripheral ganglia and jaws, thus facilitating predation
and expansion of the brain. We recently identified a “cranial-specific” neural crest transcriptional
subcircuit in jawed vertebrates (gnathostomes) that imbues this neural crest population with the
unique ability, absent from trunk neural crest, to form craniofacial cartilage that is critical for jaw
formation. Here, we propose to examine whether homologous genes are expressed in the
cranial premigratory neural crest of lamprey, a jawless basal vertebrate (agnathan). Our
preliminary results suggest that many of these genes are “missing” from the lamprey's
premigratory cranial neural crest, thus challenging the hypothesis that invention of neural crest
in vertebrates gave rise to a “New Head”. Accordingly, we hypothesize that there was
progressive expansion of neural crest derivatives during the course of vertebrate evolution. This
likely occurred by addition of new enhancer elements into the premigratory neural crest that
conferred novel developmental potential onto this cell population. As case in point, lamprey lack
a vagal neural crest that in gnathostomes forms the enteric nervous system. To test this
hypothesis, we will perform lineage analysis, analyze transcription factors and regulatory
regions of selected genes across agnathan and gnathostomes. We will identify putative
enhancers, dissect their regulatory inputs, and test the ability of these regions to drive reporter
expression in lamprey as well as cross-species, in the zebrafish. The results promise to
elucidate how new cell types arose during vertebrate evolution under the umbrella of the neural
crest.

Grant Number: 5R35NS111564-07
NIH Institute/Center: NIH
Principal Investigator: Marianne Bronner