The origin and evolution of vertebrate neural crest cells.

Joshua R York,David W Mccauley

doi:10.1098/rsob.190285

Abstract

The neural crest is a vertebrate-specific migratory stem cell population that generates a remarkably diverse set of cell types and structures. Because many of the morphological, physiological and behavioural novelties of vertebrates are derived from neural crest cells, it is thought that the origin of this cell population was an important milestone in early vertebrate history. An outstanding question in the field of vertebrate evolutionary-developmental biology (evo-devo) is how this cell type evolved in ancestral vertebrates. In this review, we briefly summarize neural crest developmental genetics in vertebrates, focusing in particular on the gene regulatory interactions instructing their early formation within and migration from the dorsal neural tube. We then discuss how studies searching for homologues of neural crest cells in invertebrate chordates led to the discovery of neural crest-like cells in tunicates and the potential implications this has for tracing the pre-vertebrate origins of the neural crest population. Finally, we synthesize this information to propose a model to explain the origin of neural crest cells. We suggest that at least some of the regulatory components of early stages of neural crest development long pre-date vertebrate origins, perhaps dating back to the last common bilaterian ancestor. These components, originally directing neuroectodermal patterning and cell migration, served as a gene regulatory ‘scaffold' upon which neural crest-like cells with limited migration and potency evolved in the last common ancestor of tunicates and vertebrates. Finally, the acquisition of regulatory programmes controlling multipotency and long-range, directed migration led to the transition from neural crest-like cells in invertebrate chordates to multipotent migratory neural crest in the first vertebrates.

Highlights

The origin of the vertebrates some 500 Ma was a milestone in early animal evolution that has since led to the diversification of over 69 000 extant species as well as countless others described from the fossil record [1]
Neural crest cells form in the dorsal-most part of the nascent embryonic central nervous system (CNS), from which they detach and migrate throughout the embryo to give rise to a diverse array of cell types that go on to make up many of the morphological and physiological traits that characterize the vertebrate clade, including most of the craniofacial skeleton and peripheral sensory nervous system, striking patterns of pigmentation, components of the teeth, heart and endocrine system, and much more [9,10,11]
Because most of these traits are hallmarks head skeleton skin colour jaws teeth heart nervous system neural crest stem cell of the vertebrate body plan, the origin of the neural crest is thought to have been a seminal event in early vertebrate history because it enabled a series of evolutionary transitions that distinguished the vertebrates from their invertebrate chordate relatives [12,13,14,15,16]

Summary

Introduction

The origin of the vertebrates some 500 Ma was a milestone in early animal evolution that has since led to the diversification of over 69 000 extant species as well as countless others described from the fossil record [1]. Neural crest cells form in the dorsal-most part of the nascent embryonic central nervous system (CNS), from which they detach and migrate throughout the embryo to give rise to a diverse array of cell types that go on to make up many of the morphological and physiological traits that characterize the vertebrate clade, including most of the craniofacial skeleton and peripheral sensory nervous system, striking patterns of pigmentation, components of the teeth, heart and endocrine system, and much more [9,10,11] (figures 1 and 2). We summarize briefly the developmental genetics of migratory neural crest stem cells in vertebrates and use this information within a comparative framework to trace the origins of neural crest-like cells in invertebrates and to build a model to account for the stepwise evolution of regulatory mechanisms driving the production of migratory and multipotent neural crest cells in the first vertebrates

Neural crest developmental genetics in vertebrates:

Insights from invertebrates into the evolution of neural crest cells

Tunicates

Ancient origins of neural crest regulatory mechanisms

52. Moreno-Bueno G et al 2006 Genetic profiling of

94. Bourlat SJ et al 2006 Deuterostome phylogeny