The evolution and elaboration of vertebrate neural crest cells

Vertebrate neural crest cells are embryonic neuroepithelial cells that undergo an epithelial–mesenchymal transition, migrate throughout the embryo and form a wide variety of derivatives, including peripheral neurons and glia, pigment cells, and craniofacial cartilage, bone and teeth. Neural crest cell evolution and elaboration is intimately bound up with vertebrate evolution: the most primitive living vertebrates, lampreys and hagfishes, have most but not all neural crest derivatives. A torrent of recent molecular information has changed our understanding of vertebrate phylogenetic relationships, expanded our understanding of the gene circuitry underlying neural crest development, and given interesting information on the deployment of homologues of these genes in invertebrate relatives such as ascidians and amphioxus. New molecular insights into the evolutionary origin of cartilage, as well as into the nature and evolution of the cells and genes involved in tooth and bone formation, enable tentative hypotheses to be framed for the evolution of skeletal neural crest derivatives.

Introduction

Vertebrate neural crest cells are a transient population of embryonic cells that arise at the lateral borders of the neural plate, undergo an epithelial–mesenchymal transition in a rostrocaudal wave as the neural tube closes, and migrate into the periphery as a heterogeneous population of multipotent and fate-restricted cells (Figure 1). They differentiate to form an astonishing diversity of cell types, including sensory, sympathetic, parasympathetic and enteric neurons, Schwann cells and satellite glia, pigment cells, chemosensory cells, endocrine cells, smooth muscle, adipocytes, craniofacial cartilage, bone and dentine-producing odontoblasts.

Twenty-five years ago, Northcutt and Gans proposed that most vertebrate-specific characters arise from neural crest and cranial placodes (transient patches of thickened embryonic head ectoderm that form the paired peripheral sense organs, a multitude of different afferent neurons and the endocrine adenohypophysis; see [1]), together with a muscularised pharynx [2, 3]. They suggested that neural crest and cranial placodes evolved in association with a transition from filter-feeding through ciliated slits in the pharynx (fore-gut), to suction feeding and eventually active predation using a muscularised pharynx as a pump, with pharyngeal slits modified for gill-based respiration [2, 3]. Thus, the staggering variety of neural crest and cranial placode derivatives could be rationalised as adaptations for a mobile, predatory lifestyle, with subsequent elaboration.

Neural crest and cranial placodes both originate from ectoderm at the neural plate border, and form many similar cell types, but there are fundamental differences in their development that make a common evolutionary origin very unlikely [4^•]. The generation of credible hypotheses for neural crest evolution needs an accurate phylogenetic framework, a comprehensive understanding of the gene regulatory networks underlying neural crest development, and information on the roles of homologues of those genes in vertebrate sister taxa, such as ascidians and amphioxus. Over the last several years, an explosion of molecular information has revolutionised our understanding of chordate relationships, dramatically advanced our knowledge of the genetic regulation of neural crest development, and given fascinating insights into how neural crest cells may have evolved and been elaborated.