Heterochronic shift between early organogenesis and migration of cephalic neural crest cells in two divergent evolutionary phenotypes of archosaurs: crocodile and ostrich

Living archosaurs (crocodiles and birds) represent an intriguing evo-devo model system. Although close in phylogenetic relationship, the two lineages show considerable divergence in trends of phenotypic evolution. The head anatomy of recent crocodilians has changed little in comparison with that of their crocodylomorph ancestors. The head phenotype of the avians (birds), as well as some non-avian theropods, shows numerous evolutionary innovations that differ considerably from the crocodylomorph pattern. Most of the novel head structures, such as features of the craniofacial skeleton, cranial nerves, head muscles, and integument are derived from the same cellular source common to all archosaurs, the cephalic neural crest (CNC). Therefore, other factors must be involved in the developmental disparity of homologous structures in the aforementioned lineages. The present study analyzes the earliest developmental events that are associated with the appearance of the neural crest cells in the two archosaur models: Crocodylus niloticus and Struthio camelus. I found that both models share unique developmental features, the presence of an unpaired, rostrally migrating population of CNC cells, showing that the two are closely related to each other. On the other hand, the crocodile and the ostrich differ substantially in (1) timing, (2) duration, and (3) expression patterns of the CNC. Compared with the crocodile, the CNC cells in the ostrich (1) migrate much later into the embryonic head, (2) but relocate to their terminal positions faster, and (3) take specifically directed migratory routes in the mandibular/oral region and head/trunk-interface regions. I suggest that accelerated relocation of CNC cells combined with delayed head organogenesis may represent important innovative conditions in the developmental evolution of a new archosaur head phenotype.