Abstract:
Thanks to their cellular and genomic simplicity, tunicate embryos are ideally suited for the study of developmental genetics at single-cell resolution. As the invertebrates most closely related to us, they have helped shed light on the origins and development of many chordate- or vertebrate-specific features such as the notochord, gills, spinal cord, jaw muscles, liver, thyroid, and many others. One of the most important vertebrate features is the Neural Crest, a population of migratory, multipotent progenitors that give rise to multiple cell types, tissues, and structures including most of our cranium. However, its evolutionary origins are obscured by a lack of convincing homologs outside the vertebrates, other than the neural plate border-derived pigment cells of tunicates and cephalochordates. We show that a particular neuronal cell type in the tunicate larva, the Bipolar Tail Neuron (BTN), shares a set of traits with Neural Crest-derived Dorsal Root Ganglia neurons. BTNs derive from caudal neural plate border cells, delaminate, and migrate along the paraxial mesoderm on either side of the neural tube, eventually differentiating into afferent neurons that form synaptic contracts with both epidermal sensory cells and motor neurons. We propose that the neural plate borders of the chordate ancestor already produced both migratory peripheral neurons and pigment cells. This would suggest that the Neural Crest evolved through the acquisition of a multipotent, stem cell-like regulatory state upstream of multiple, pre-existing neural plate border cell differentiation programs.