Abstract

SummaryFor well over half of the 150 years since the discovery of the neural crest, the special ability of these cells to function as a source of species‐specific pattern has been clearly recognized. Initially, this observation arose in association with chimeric transplant experiments among differentially pigmented amphibians, where the neural crest origin for melanocytes had been duly noted. Shortly thereafter, the role of cranial neural crest cells in transmitting species‐specific information on size and shape to the pharyngeal arch skeleton as well as in regulating the timing of its differentiation became readily apparent. Since then, what has emerged is a deeper understanding of how the neural crest accomplishes such a presumably difficult mission, and this includes a more complete picture of the molecular and cellular programs whereby neural crest shapes the face of each species. This review covers studies on a broad range of vertebrates and describes neural‐crest‐mediated mechanisms that endow the craniofacial complex with species‐specific pattern. A major focus is on experiments in quail and duck embryos that reveal a hierarchy of cell‐autonomous and non‐autonomous signaling interactions through which neural crest generates species‐specific pattern in the craniofacial integument, skeleton, and musculature. By controlling size and shape throughout the development of these systems, the neural crest underlies the structural and functional integration of the craniofacial complex during evolution.

Highlights

  • The notion that neural crest cells generate species-specific pattern has a long and colorful history

  • The dermis specifies the pattern through which epidermis forms feather buds by adhering to the timetable of the donor species and by defining the expression domains of members and targets of the Sonic Hedgehog (SHH), Bone Morphogenetic Protein (BMP), and Delta/Notch pathways (Eames & Schneider, 2005). This remarkable capacity holds true in reverse as evidenced by duail chimeras where slower-developing duck dermis acts out its feather program on a delayed timetable relative to quail host epidermis and produces duck-like feathers. Extrapolating these results, we would predict that the dermis most likely regulates in a species-specific manner many other genes known to function during feather morphogenesis such as members and targets of the Fibroblast Growth Factor (FGF), Epidermal Growth Factor, and WNT pathways (Atit, Conlon, & Niswander, 2003; Chang et al, 2004; Chodankar et al, 2003; Mandler & Neubuser, 2004; Noji et al, 1993; Noramly, Freeman, & Morgan, 1999; Olivera-Martinez, Thelu, Teillet, & Dhouailly, 2001; Rouzankina, Abate-Shen, & Niswander, 2004; Song, Wang, & Goetinck, 1996; Song, Lee, & Goetinck, 2004; Tanda, Ohuchi, Yoshioka, Noji, & Nohno, 1995; Tao et al, 2002; Widelitz, Jiang, Chen, Stott, & Chuong, 1999; Widelitz, Jiang, Noveen, Chen, & Chuong, 1996)

  • While the sequential stages of chondrogenesis are comparable in quail and duck, in quck chimeras, we find that quail donor neural crest cells make smaller condensations and differentiate into cartilage on a faster timetable

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Summary

Summary

For well over half of the 150 years since the discovery of the neural crest, the special ability of these cells to function as a source of species-specific pattern has been clearly recognized. This observation arose in association with chimeric transplant experiments among differentially pigmented amphibians, where the neural crest origin for melanocytes had been duly noted. A major focus is on experiments in quail and duck embryos that reveal a hierarchy of cell-autonomous and non-autonomous signaling interactions through which neural crest generates species-specific pattern in the craniofacial integument, skeleton, and musculature. KEYWORDS cranial neural crest, craniofacial development, evolutionary-developmental biology, quail-duck chimeras, quck, species-specific pattern, tissue-interactions

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