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Evolutionary Origins of the Neural Crest and Neural Crest Cells

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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 220:268-274, 1983. doi:10.1126/science.220.4594.268; Northcutt and Gans The Quarterly Review of Biology 58:1–28, 1983. doi:10.1086/413055). I outline the rationale behind the new head hypothesis before turning to an examination of the pivotal role played by NCCs in the evolution of pharyngeal arches, in the context of the craniofacial skeleton. Integrations between the evolving vertebrate brain, muscular pharynx and paired sensory organs may have necessitated that the pharyngeal arch skeletal system—and subsequently, the skeleton of the jaws and much of the skull (the first vertebrates being jawless)—evolved from NCCs whose developmental connections were to neural ectoderm and neurons rather than to mesoderm and connective tissue; mesoderm produces much of the vertebrate skeleton, including virtually all the skeleton outside the head. The origination of the pharyngeal arch skeleton raises the issue of the group of organisms in which and how cartilage arose as a skeletal tissue. Did cartilage arise in the basal proto-vertebrate from a single germ layer, cell layer or tissue, or were cells and/or genes co-opted from several layers or tissues? Two recent studies utilizing comparative genomics, bioinformatics, molecular fingerprinting, genetic labeling/cell selection, and GeneChip Microarray technologies are introduced as powerful ways to approach the questions that are central to this review.

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Notes

  1. As this review deals with the origination rather than the evolution of diversification and specialization of neural crest cells, I do not discuss the evidence for neural crest cells and their derivatives in lampreys and hagfishes, nor do I discuss the phylogenetic relationships between lampreys and hagfishes. For entrees into the literatiure on these topics, see Kuratani et al. (2002), Meulemans and Bronner-Fraser (2002), Janvier (2007), Ota and Kuratani 2006, 2007, and Ota et al. (2007).

  2. For many years, Col2a1 has been regarded as the “cartilage collagen gene”. However, we will see that Col2a1 is expressed in the notochord and in endodermal cells. Furthermore, many NCCs express Col2a1, often in combination with genes such as Sox9, Sox10, and LSox5, which activate the collagen gene. So general is this combination of gene expressions that Suzuki et al. (2006)) concluded that Col2a1 is a “general mesenchyme gene.”.

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Acknowledgments

I thank Ryan Kearney, Daniel Meulemans and the two anonymous reviewers for constructive comments on the paper, an expanded version of which (including additional literature and discussion of the origin of jaws) will appear as Chapter 4 in Hall (2008a). Research support from the Natural Sciences and Engineering Research Council of Canada (grant # A5056) is gratefully acknowledged.

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  1. Department of Biology, Dalhousie University, Halifax, NS, Canada, B3H 4J1

    Brian K. Hall

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Hall, B.K. Evolutionary Origins of the Neural Crest and Neural Crest Cells. Evol Biol 35, 248–266 (2008). https://doi.org/10.1007/s11692-008-9033-8

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