Neural crest contribution to the avian shoulder girdle and implications to girdle evolution in vertebrates

Abstract

Neural crest (NC) is an established source for many endochondral and intramembranous bones in the skull and postcranial skeleton in vertebrates. Neural crest cells also contribute to the trapezius/cleidohyoideus muscle attachment sites on the shoulder girdle of the mouse, where they are found in the scapula, clavicle, and sternum. In the avian shoulder girdle, NC cells from the level of the first two cranial−most somites were only found so far in the clavicle, while in the axolotl, the NC contribution to the shoulder girdle was not found at all. In this study we aimed to determine whether NC cells caudal to the level of the second somite contribute to the cartilaginous shoulder girdle in birds and to analyse the phylogenetic distribution of NC cells in the vertebrate shoulder girdle. Homotopic quail to chick embryos and GFP+ to white chick embryos transplantations of the neural tube including presumptive NC, as well as immunohistochemical detection of NC markers, such as HNK-1 and PDGFRα revealed no contribution of NC cells from somite levels 3−27 to the skeletal elements of the shoulder girdle, including, but not restricting to muscle attachment sites, despite abundance of other NC derivatives. Thus, in birds, NC does not contribute to the formation of the cartilaginous shoulder girdle. The negative result is discussed in a broad evolutionary aspect. It supports the notion of the uniqueness of NC contribution to the variety of endochondral bones in mice (or mammals). In other vertebrates, including birds, only the cells of the cranial NC seem to migrate to the shoulder girdle and contribute to the intramembranous clavicles and/or interclavicle. We critically evaluate the existing hypotheses on evolution of NC contribution to the shoulder girdle in vertebrates.