Abstract
BackgroundA major step during the evolution of tetrapods was their transition from water to land. This process involved the reduction or complete loss of the dermal bones that made up connections to the skull and a concomitant enlargement of the endochondral shoulder girdle. In the mouse the latter is derived from three separate embryonic sources: lateral plate mesoderm, somites, and neural crest. The neural crest was suggested to sustain the muscle attachments. How this complex composition of the endochondral shoulder girdle arose during evolution and whether it is shared by all tetrapods is unknown. Salamanders that lack dermal bone within their shoulder girdle were of special interest for a possible contribution of the neural crest to the endochondral elements and muscle attachment sites, and we therefore studied them in this context.ResultsWe grafted neural crest from GFP+ fluorescent transgenic axolotl (Ambystoma mexicanum) donor embryos into white (d/d) axolotl hosts and followed the presence of neural crest cells within the cartilage of the shoulder girdle and the connective tissue of muscle attachment sites of the neck-shoulder region. Strikingly, neural crest cells did not contribute to any part of the endochondral shoulder girdle or to the connective tissue at muscle attachment sites in axolotl.ConclusionsOur results in axolotl suggest that neural crest does not serve a general function in vertebrate shoulder muscle attachment sites as predicted by the “muscle scaffold theory,” and that it is not necessary to maintain connectivity of the endochondral shoulder girdle to the skull. Our data support the possibility that the contribution of the neural crest to the endochondral shoulder girdle, which is observed in the mouse, arose de novo in mammals as a developmental basis for their skeletal synapomorphies. This further supports the hypothesis of an increased neural crest diversification during vertebrate evolution.
Highlights
The vertebrate shoulder girdle is a complex structure consisting of endochondral and dermal skeletal elements
Experiments with quail-chick chimeras were the first that established a somitic contribution to the endochondral scapula in addition to the material of the lateral plate mesoderm, which forms the rest of the endochondral shoulder girdle [1,2]
The caudally migrating neural crest cells from the level of rhombomeres 6 and 7 and somites 1 and 2, form the cranialmost medial part of the dermal clavicle, e.g., connective tissue at the site of attachment of the cleidohyoid muscle, which connects the clavicle to the tongue skeleton [4,5]
Summary
The vertebrate shoulder girdle is a complex structure consisting of endochondral and dermal skeletal elements. The endochondral part of the shoulder girdle and the limb skeleton were long considered to be derived solely from lateral plate mesoderm, whereas the dermal part of the shoulder girdle was regarded as neural crest derived. A major step during the evolution of tetrapods was their transition from water to land This process involved the reduction or complete loss of the dermal bones that made up connections to the skull and a concomitant enlargement of the endochondral shoulder girdle. In the mouse the latter is derived from three separate embryonic sources: lateral plate mesoderm, somites, and neural crest. Salamanders that lack dermal bone within their shoulder girdle were of special interest for a possible contribution of the neural crest to the endochondral elements and muscle attachment sites, and we studied them in this context
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