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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.

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Fig. 1: Core elements of the new head hypothesis.
Fig. 2: Neural crest development and gene regulatory networks.
Fig. 3: Evolution of neural crest features throughout deuterostome evolution.

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Acknowledgements

The authors thank J. Stundl for comments and discussion on this manuscript. This work was supported by the US National Institutes of Health (NIH) grant R35NS111564 to M.E.B. M.L.M. was supported by a fellowship from the Helen Hay Whitney Foundation and by NIH grant 1K99HD100587.

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Correspondence to Marianne E. Bronner.

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Glossary

Chordates

Animals of the phylum Chordata that possess a notochord, dorsal nerve cord, endostyle or thyroid, gill slits and a tail. This phylum includes amphioxus, ascidians and vertebrates.

Synapomorphy

A shared, derived trait of two or more groups that was present in a last common ancestor.

Cranial neural crest

The anterior-most subpopulation of the neural crest that gives rise to a large majority of the craniofacial skeleton, melanocytes and cranial ganglia.

Vagal neural crest

A subpopulation of neural crest cells arising from somites 1–7 that contributes to the enteric nervous system and cardiovascular derivatives.

Trunk neural crest

A subpopulation of neural crest cells that originates from somites 8–28 and forms neurons and glia of the dorsal root ganglia and sympathetic nervous system as well as melanocytes.

Lumbosacral neural crest

The posterior-most subpopulation of the neural crest that gives rise to portions of the enteric and sympathetic nervous systems.

Gnathostomes

Jawed vertebrates that include all vertebrates except cyclostomes.

Cyclostomes

Jawless vertebrates and sister group to the gnathostomes that include hagfish and sea lamprey.

Deuterostomes

Animals of the superphylum Deuterostomia that form their anus before their mouth during development. This superphylum includes animals such as sea urchins, amphioxus, ascidians and all vertebrates.

Urochordates

Animals of the chordate subphylum Urochordata, which includes tunicates (also known as ascidians).

Cephalochordate

An animal of the chordate subphylum Cephalochordata, which includes lancelets (also known as amphioxus).

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Martik, M.L., Bronner, M.E. Riding the crest to get a head: neural crest evolution in vertebrates. Nat Rev Neurosci 22, 616–626 (2021). https://doi.org/10.1038/s41583-021-00503-2

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