Evolutionary Origins of the Neural Crest and Neural Crest Cells

Abstract

I evaluate the lines of evidence-cell types, genes, gene pathways, fossils-in putative chordate ancestors-cephalochordates and ascidians-pertaining to the evolutionary origin of the vertebrate neural crest. Given the intimate relationship between the neural crest and the dorsal nervous system during development, I discuss the dorsal nervous system in living (extant) members of the two groups, especially the nature, and genes, and gene regulatory networks of the brain to determine whether any cellular and/or molecular precursors (latent homologues) of the neural may have been present in ancestral cephalochordates or urochordates. I then examine those fossils that have been interpreted as basal chordates or cephalochordates to determine whether they shed any light on the origins of neural crest cell (NCC) derivatives. Do they have, for example, elements of a head skeleton or pharyngeal arches, two fundamental vertebrate characters (synapomorphies)? The third topic recognizes that the origin of the neural crest in the first vertebrates accompanied the evolution of a brain, a muscular pharynx, and paired sensory organs. In a paradigm-breaking hypothesis-often known as the 'new head hypothesis'-Carl Gans and Glen Northcutt linked these evolutionary innovations to the evolution of the neural crest and ectodermal placodes (Gans and Northcutt Science 220: [268][269][270][271][272][273][274] 1983.

The evolutionary and genetic origins of consciousness in the Cambrian Period over 500 million years ago

“…Although the urochordate brain has become specialized and even reduced, Glover and Fritzsch (2009) say it evolved from a more advanced ancestral brain because its bulged sub-parts are more distinct than in the un-bulged, uniformly tube-shaped brain of cephalochordates (compare Figures 2A,B). Further, while it was long supposed that cephalochordates are the closest relatives (sister group) of the vertebrates, more recent molecular-phylogenetic analyses suggest that urochordates instead are the sister group of vertebrates and that the cephalochordates arose earlier (Bourlat et al, 2006; Delsuc et al, 2006; Holland, 2007; Hall, 2008; Lacalli, 2008b; Lamb, 2011; Figure 1). …”

“…Perhaps the single most important innovation marking this transition to vertebrates was the appearance of neural crest and neural placodes (Gans and Northcutt, 1983; Northcutt, 1996a,b, 2005; Hall, 2008; Sauka-Spengler and Bronner-Fraser, 2008). The neural plate is a region of thickened ectoderm that forms longitudinally on the dorsal surface of the developing vertebrate embryo (Figure 3).…”

“…The neural plate is a region of thickened ectoderm that forms longitudinally on the dorsal surface of the developing vertebrate embryo (Figure 3). Then, double-walled folds form at the anterior and lateral regions of the neural plate, the inner walls of which give rise to the neural crest cells while the lateral folds give rise to the ectodermal or neurogenic placodes (Allman, 1999; Holland and Chen, 2001; Holland and Holland, 2001; Baker, 2005; Schlosser, 2005, 2008; Donoghue et al, 2008; Hall, 2008, 2009; Graham and Shimeld, 2012). …”

“…The neurons in the trigeminal ganglion (cranial nerve V) that transmit sensations of touch, pain, and temperature from the face are of combined neural crest and placodal origin, and the neurons of the facial, glossopharyngeal, and vagus nerves that provide afferent innervation for the taste buds are of placodal origin. Indeed, the entire peripheral nervous system is derived from cells that originate within the neural crest and cranial placodes (Holland and Holland, 2001; Baker, 2005; Schlosser, 2005, 2008, 2010; Donoghue et al, 2008; Hall, 2008, 2009; Graham and Shimeld, 2012). A minor exception is that all life stages of lampreys, and the larvae of fish and amphibians, retain a few non-crest-derived sensory neurons called Rohon-Beard cells.…”

“…In protochordates, particularly urochordates, candidate placode- and crest-like cells have been identified, and there is some expression of placode- and crest-specific genes in both cephalochordates and urochordates (Holland and Holland, 2001; Donoghue et al, 2008; Hall, 2008; Holland et al, 2008; Schlosser, 2008; Glover and Fritzsch, 2009; Yu, 2010; Graham and Shimeld, 2012). Recently, Abitua et al (2012) found the best candidate for a neural-crest homologue in the pigment-forming “A9.49” cells of tunicates, but these cells do not migrate nor form any ectomesenchyme as true crest cells do.…”