Riding the crest to get a head: neural crest evolution in vertebrates

Abstract

In their seminal 1983 paper, Gans and Northcutt proposed that evolution of the vertebrate 'new head' was made possible by the advent of the neural crest and cranial placodes. The neural crest is a stem cell population that arises adjacent to the forming CNS and contributes to important cell types, including components of the peripheral nervous system and craniofacial skeleton and elements of the cardiovascular system. In the past few years, the new head hypothesis has been challenged by the discovery in invertebrate chordates of cells with some, but not all, characteristics of vertebrate neural crest cells. Here, we discuss recent findings regarding how neural crest cells may have evolved during the course of deuterostome evolution. The results suggest that there was progressive addition of cell types to the repertoire of neural crest derivatives throughout vertebrate evolution. Novel genomic tools have enabled higher resolution insight into neural crest evolution, from both a cellular and a gene regulatory perspective. Together, these data provide clues regarding the ancestral neural crest state and how the neural crest continues to evolve to contribute to the success of vertebrates as efficient predators.

Figure 1.. Core elements of the New Head Hypothesis.

New Head hypothesis proposed that the complexity and elaboration of the vertebrate head was a consequence of the advent of the migratory cranial neural crest and cranial placodes. These new cell types enabled assembly of the craniofacial skeleton and a novel sensory system, which in turn allowed expansion of the anterior neuroepithelium into the vertebrate brain. The morphological characters that arise from the neural crest and cranial placodes also allowed for the transition from a predominantly filter feeding lifestyle of invertebrate chordates to active predation of vertebrates. During development, the cranial neural crest will emigrate from the neural tube to populate the forming head (a). Distinct neural crest migratory pathways are color coded to match the craniofacial skeleton derivatives they will form in the adult (b) (adapted from Couly et al, 1998 and Santagati and Rijli, 2003)^,. Formation of the cranial placodes (c) is also a defining feature of the vertebrate New Head (adapted from Depew and Olsson, 2008) .

Figure 2.. Neural crest development and gene regulatory networks.

(a.) Developmental milestones of neural crest formation include formation of the neural plate border, specification of the neural crest, delamination from the central nervous system, and migration to often distant locations to give rise to diverse cell types (adapted from Martik and Bronner, 2017) . (b.) Along the anteriorposterior body axis, the neural crest is broken into four main subpopulations: the cranial, vagal, trunk, and sacral. Dotted line (a) represents location of the section depicted in panel a. (c.) Depending on their final axial location, the neural crest will differentiate into unique derivatives. (d.) Underlying the development of the neural crest is a pan-neural crest gene regulatory network that is composed of hierarchically organized modules of signaling molecules and transcription factors that dictate each process. Regulatory information gleaned from neural crest-like cells in tunicates have now enabled the investigation into neural crest-like cell type evolution (adapted from Green, et al, 2015) .

Figure 3.. Cladogram of extant deteurostome neural crest-related characters and evolution.

Presented is a model for the evolution of neural crest features throughout deuterostome evolution. Labels to the right indicate monophyletic groupings. Highlighted character changes within a stem group are listed by bullet points. Animal illustrations adapted from Martik, et al 2019 or Biorender.com.