The neural crest is an embryonic cell population that gives rise to an array of tissues and structures in adult vertebrates including most of the head skeleton. Because neural crest cells (NCCs), and many of their derivatives, are unique to vertebrates, the evolution of the neural crest is thought to have potentiated vertebrate origins and diversification. However, the lack of clear NCC homologs in invertebrate chordates has made it difficult to reconstruct the evolutionary history of modern NCCs. In this review, the development of NCCs in the basal jawless vertebrate, lamprey, is compared with the development of neural crest-like cells in a range of invertebrates to deduce features of the first NCCs and their evolutionary precursors. These comparisons demonstrate that most of the defining attributes of NCCs are widespread features of invertebrate embryonic ectoderm. In addition, they suggest ancient origins for the neural border domain and chondroid skeletal tissue in the first bilaterian, and show that NCCs must have evolved in a chordate with an unduplicated invertebrate-type genome. On the basis of these observations, a stepwise model for the evolution of NCCs involving heterotopic and heterochronic activation of ancient ectodermal gene programs and new responsiveness to preexisting inducing signals is proposed. In light of the phylogenetic distribution of neural crest-like cells, the deep homology of developmental gene networks, and the central role of evolutionary loss in deuterostome evolution, this article concludes with suggestions for future studies in a broad range of bilaterians to test key aspects of this model. WIREs Dev Biol 2013, 2:1-15. doi: 10.1002/wdev.85 For further resources related to this article, please visit the WIREs website.
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