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WIREs Dev Biol
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The evolution of the neural crest: new perspectives from lamprey and invertebrate neural crest‐like cells

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Abstract 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 This article is categorized under: Early Embryonic Development > Development to the Basic Body Plan Comparative Development and Evolution > Organ System Comparisons Between Species Comparative Development and Evolution > Evolutionary Novelties

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Lamprey neural crest cell (NCC) development. (a–c) Pre‐migratory neural crest cells during neurulation in lamprey from Damas, 1944.20 (d) NCCs migrating in streams visualized by in situ hybridization for an Endothelin receptor in a lamprey embryo after neurulation. (e) Neural crest derivatives in a lamprey ammocoete larva. Light blue is mucocartilage, blue is cellular cartilage, dark blue is cranial ganglia, purple is dorsal root ganglia, orange is dorsal fin mesenchyme, and the white box highlights melanocytes.

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Chordate phylogeny. The cyclostomes, lamprey and hagfish, are living agnathans, a group that includes the ostracoderms, fossil jawless fish with bony dermal armor. Shown here are two major ostracoderm groups, the osteostracans and heterostracans. The neural crest (NC), in its modern form, was present in the last common ancestor of all living vertebrates. The two vertebrate whole genome duplications (GD) likely occurred after the evolution of the neural crest (see main text), but their timing relative to the divergence of gnathostomes and agnathans is currently unresolved.

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A stepwise model for the evolution of neural crest cells. (a) The first chordate likely had a diffuse general‐ectoderm‐derived peripheral nervous system (PNS) consisting of both migratory and non‐migratory sensory cell types. Mitf‐expressing melanocytes formed in the central nervous system, and a mesendoderm‐derived, chondroid skeletal tissue supported the pharynx. (b) Reorganization of the PNS results in the concentration of migratory sensory cells in the neural border domain, and mostly non‐migratory sensory cells in the dorsal anterior ectoderm. (c) Heterochronic migration of uncommitted neural border precursors leads to a bi‐potent proto‐neural crest cell (NCC) population capable of generating both sensory cells and melanocytes. (d) Migration of uncommitted neural border precursors into the pharynx exposes them to skeletogenic signals, like FGFs, inducing the secretion of skeletal matrix by these cells. These early skeletogenic NCC contributed to the mesendoderm‐derived pharyngeal skeleton. (e) In the first vertebrates, the pharyngeal skeleton is almost totally replaced by skeletogenic NCCs. Duplication of neural crest gene regulatory network components occurred sometime after the appearance of skeletogenic NCCs.

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The phylogenetic distribution of cells with neural crest‐like properties in the bilateria. MN, delaminating and migrating neuroblast; CC, cellular cartilage; NB, neural border; MM, migratory multipotent cells; MP, migratory pigment cells; AC, acellular collagenous cartilage.

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Combinatorial expression of Pax3/7, Msx, and Dlx defines the border of the neural and general ectoderm in chordates and annelids. Neural crest cellS (NCCs) in vertebrates and Rhode sensory cells in amphioxus arise from the Dlx‐free, Pax3/7/Msx‐positive portion of the chordate neural border. Cranial placodes in vertebrates and midline sensory cells in urochrodates are derived from the adjacent ectoderm, which coexpresses Pax3/7, Msx, and Dlx. In annelids, sensory cells also form from a strip of Pax3/7/Msx/Dlx‐positive ectoderm immediately adjacent to a Pax3/7/Msx‐positive domain.

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Comparative Development and Evolution > Organ System Comparisons Between Species
Comparative Development and Evolution > Evolutionary Novelties
Early Embryonic Development > Development to the Basic Body Plan