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

Abstract

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.

Comparative anatomy and development of pectoral and pelvic girdles in hylid anurans

“…In anurans, only one muscle, the levator scapulae superior, is attached to the single cervical vertebra (the atlas). Thus, this muscle is more closely associated with the neck than is the cucullaris, which is probably a head muscle (Nagashima et al, ). The levator scapulae receives motor supply from the cervical plexus (Frank, Wenk, Stern, Gottlieb, & Moscatello, ).…”

Neural crest and the patterning of vertebrate craniofacial muscles

“…It is well known from comparative studies that the head:trunk interface has undergone profound evolutionary changes during vertebrate evolution (reviewed by: Sefton, Bhullar, Mohaddes, & Hanken, ). Among these is the location of pectoral girdle elements, many of which initially were close to and stabilized upon an expanded dermal roof of the skull and located at the same axial levels as caudal branchial muscles and NC‐derived gill elements (reviewed by: Ferguson & Graham, ; Lours‐Calet et al, ; Oisi et al, ; Sefton et al, ), but in amniotes arise from more caudally located somites and somatic mesoderm (reviewed by Nagashima et al, ).…”

“…These results suggest that the tight, obligatory partnering that defines intra‐branchial myogenesis holds true for those myoblasts that exit the arches. This “follow the neural crest leader” model has been extrapolated to explain the avian trapezius attachment onto a band of NCr cells in the furcula, which is homologous to the clavicle (McGonnell, McKay, & Graham, ), although mapping studies show that some clavicular cells also arise from mesoderm originating at the occipital level (Nagashima et al, ).…”

Comparative anatomy of zebrafish paired and median fin muscles: basis for functional, developmental, and macroevolutionary studies

“…A similar idea has been recently advanced in the developmental work by Nagashima et al. (), who defended the idea that the pectoral appendage develops partially from the head region using a head ‘program’, whereas the pelvic appendage rather fully uses a trunk ‘program’ (Nagashima, H. pers. commun.…”