Developmental origin of the clavicle, and its implications for the evolution of the neck and the paired appendages in vertebrates

• Published in: Journal of anatomy 2016-10, Vol.229 (4), p.536-548
• Main Authors: Nagashima, Hiroshi, Sugahara, Fumiaki, Watanabe, Keisuke, Shibata, Masahiro, Chiba, Akina, Sato, Noboru
• Format: Article
• Language: English
• Subjects: Animals; Biological Evolution; Chick Embryo; Chickens; clavicle; Clavicle - embryology; development; evolution; Mesoderm - embryology; neck; Neck - embryology; Original; paired appendage; Vertebrates - embryology
• ISSN: 0021-8782; 1469-7580
• DOI: 10.1111/joa.12502

In fish, the pectoral appendage is adjacent to the head, but during vertebrate evolution a long neck region emerged via caudal relocation of the pectoral appendage. The pectoral appendage is comprised of endochondral portions, such as the humerus and the scapula, and a dermal portion, such as the clavicle, that contributes to the shoulder girdle. In the search for clues to the mechanism of the caudal relocation of the pectoral appendage, the cell lineage of the rostral lateral plate mesoderm was analyzed in chickens. It was found that, despite the long neck region in chickens, the origin of the clavicle attached to the head mesoderm ranged between 1 and 14 somite levels. Because the pectoral limb bud and the endochondral pectoral appendage developed on 15–20 and 15–24 somite levels, respectively, the clavicle‐forming region corresponds to the embryonic neck, which suggests that the relocation would have been executed by the expansion of the source of the clavicle. The rostral portion of the clavicle‐forming region overlaps the source of the cucullaris muscle, embraces the pharyngeal arches caudally, and can be experimentally replaced with the head mesoderm to form the cucullaris muscle, which implies that the mesodermal portion could have been the head mesoderm and that the clavicle would have developed at the head/trunk boundary. The link between the head mesoderm and the presumptive clavicle appears to have been the developmental constraint needed to create the evolutionarily conserved musculoskeletal connectivities characterizing the gnathostome neck. In this sense, the dermal girdle of the ganathostomes would represent the wall of the branchial chamber into which the endochondral pectoral appendage appears to have attached since its appearance in evolution.