Incremental evolution of the neural crest, neural crest cells and neural crest‐derived skeletal tissues

Abstract

Urochordates (ascidians) have recently supplanted cephalochordates (amphioxus) as the extant sister taxon of vertebrates. Given that urochordates possess migratory cells that have been classified as 'neural crest-like' -and that cephalochordates lack such cells -this phylogenetic hypothesis may have significant implications with respect to the origin of the neural crest and neural crest-derived skeletal tissues in vertebrates. We present an overview of the genes and gene regulatory network associated with specification of the neural crest in vertebrates. We then use these molecular data -alongside cell behaviour, cell fate and embryonic context -to assess putative antecedents (latent homologues) of the neural crest or neural crest cells in ascidians and cephalochordates. Ascidian migratory mesenchymal cells -non-pigment-forming trunk lateral line cells and pigment-forming 'neural crest-like cells' (NCLC) -are unlikely latent neural crest cell homologues. Rather, Snail-expressing cells at the neural plate of border of urochordates and cephalochordates likely represent the extent of neural crest elaboration in non-vertebrate chordates. We also review evidence for the evolutionary origin of two neural crest-derived skeletal tissues -cartilage and dentine. Dentine is a bona fide vertebrate novelty, and dentinesecreting odontoblasts represent a cell type that is exclusively derived from the neural crest. Cartilage, on the other hand, likely has a much deeper origin within the Metazoa. The mesodermally derived cellular cartilages of some protostome invertebrates are much more similar to vertebrate cartilage than is the acellular 'cartilagelike' tissue in cephalochordate pharyngeal arches. Cartilage, therefore, is not a vertebrate novelty, and a welldeveloped chondrogenic program was most likely co-opted from mesoderm to the neural crest along the vertebrate stem. We conclude that the neural crest is a vertebrate novelty, but that neural crest cells and their derivatives evolved and diversified in a step-wise fashion -first by elaboration of neural plate border cells, then by the innovation or co-option of new or ancient metazoan cell fates.

Insights into neural crest development and evolution from genomic analysis

“…This idea was put forward in the ''New Head'' hypothesis by Gans and Northcutt, which postulated that the emergence of neural crest derivatives allowed for remodeling of the chordate head and resulted in a shift from filter feeding to active predation (Gans and Northcutt 1983). Although the main premise of the New Head hypothesis is still supported by evidence from the fossil record and developmental studies, tracing the origin of the neural crest to an invertebrate precursor cell type has proven to be a challenge, as invertebrate chordates lack migratory cells that are formed at the neural plate border (Northcutt 2005;Hall and Gillis 2013;Medeiros 2013). Assessment of the regulatory identity of the neural crest and its putative evolutionary precursors holds the promise of shedding light on the evolutionary origins of the vertebrate neural crest.…”

“…This cell lineage, which is known as the trunk lateral cells, expresses the HNK-1 epitope as well as the Twist, FoxD, AP2, and Myc orthologs ( Jeffery 2006;Jeffery et al 2008). Further studies are necessary to determine unequivocally if these cells are derived from the neural plate border, neural tube, or other tissue (Hall and Gillis 2013). In an intriguing recent study, Abitua et al (2012) showed that a lineage a9.49 in Ciona intestinalis expresses ID, Snail, ETS, and FoxD, as well as melanogenic genes like MITF, TYR, and TYRP.…”

“…Given the sheer number of cell types and derivatives formed by the neural crest progenitor cell population and the complexity of its developmental program, it is not surprising that a large fraction of congenital birth defects can be traced back to the neural crest (Hall 1999). Neural crest developmental anomalies, or neurocristopathies, are responsible for the vast majority of craniofacial malformations, and more than 700 different syndromes have been described (Trainor 2010).…”

“…Interest in this cell population has been further fueled by its medical and evolutionary importance. For example, numerous congenital birth defects and neoplastic diseases are linked to abnormal development of the neural crest development and its derivatives (Hall 1999). Due to its inherent stem cell properties, there is great interest in using these cells in regenerative medicine to treat disorders like familial dysautonomia, cleft palate, and some heart conditions ( Jones and Trainor 2004;Lee et al 2009).…”

Quantitative genetics provides predictive power for paleontological studies of morphological evolution

“…In recent years, startling advances have been made in our understanding of the molecular mechanisms of development and the genomic structures that underpin them. Laboratory manipulations are able to determine the patterns of gene expression that produce phenotypic structures such as brains, bones, and teeth (2,3); computational models of the spatial dynamics of development are capable of predicting the phenotypic outcomes of up-or down-regulation of gene expression (4); and genomic analyses reveal the regulatory mechanisms that govern cascades of gene expression (5). These tools have mapped the causal links between genotype and phenotype that were largely missing from 20th century evolutionary biology.…”