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.

Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues

“…Wnt1 Cre and Sox10 Cre NCC reporter mice were used to show that endochondral cells connecting the cucullaris-derived muscles on the scapula, clavicle and sternum share a common NCC origin with the connective tissue (Matsuoka et al, 2005). However, NCCs are not found in pectoral components of fish, axolotl and chick, while contribution to neurocranium is conserved, suggesting that NCC involvement in shoulder formation would be specific to mammals (Epperlein et al, 2012; Kague et al, 2012; Piekarski et al, 2014; Ponomartsev et al, 2017). In contrast to this view, our lineage analysis reveals that the neural crest lineage shows limited contribution to cucullaris connective tissue and does not form endochondral cells at the posterior attachment sites (Figure 7C).…”

“…It has been suggested that NCCs form both connective tissue and endochondral cells at the attachment sites of neck muscles to shoulders in mouse (Matsuoka et al, 2005). However, studies in non-mammalian animals have contested a NCC contribution to the pectoral girdle (Epperlein et al, 2012; Kague et al, 2012; Ponomartsev et al, 2017).…”

Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues

“…513 514 Wnt1 Cre and Sox10 Cre NCC reporter mice were used to show that endochondral cells connecting 515 the cucullaris-derived muscles on the scapula, clavicle and sternum share a common NCC origin 516 with the connective tissue (Matsuoka et al, 2005). However, NCCs are not found in pectoral 517 components of fish, axolotl and chick, while contribution to neurocranium is conserved, 518 suggesting that NCC involvement in shoulder formation would be specific to mammals (Epperlein 519 23 et al, 2012; Kague et al, 2012;Piekarski et al, 2014;Ponomartsev et al, 2017). In contrast to this 520 view, our lineage analysis reveals that the neural crest lineage shows limited contribution to 521 cucullaris connective tissue and does not form endochondral cells at the posterior attachment sites 522 ( Figure 7C).…”

“…The neck and shoulder girdle contain skeletal elements and connective 111 tissues of distinct NCC, LPM or somitic origins (Durland et been suggested that NCCs form both connective tissue and endochondral cells at the attachment 114 sites of neck muscles to shoulders in mouse (Matsuoka et al, 2005). However, studies in non-115 6 mammalian animals have contested a NCC contribution to the pectoral girdle (Epperlein et al,116 2012; Kague et al, 2012;Ponomartsev et al, 2017). 117 118 Therefore, the neck region consists of muscle, skeletal and connective tissue elements of mixed 119 cellular origins, underscoring the difficulty in assigning embryonic identities for these structures.…”

Ontogenetic development of the shoulder joint muscles in frogs (Amphibia: Anura) assessed by digital dissection with implications for interspecific muscle homologies and nomenclature

“…The morphologies of the pectoral fins of fishes and of the forelimbs of tetrapods, as well as of the pectoral girdle that connects them to the axial skeleton, have long received attention to establish the homology of the anatomical elements across vertebrates and to understand the evolutionary transformations of fins into limbs and of limbs within tetrapods (e.g., Gegenbaur 1865;Rolleston 1869;Romer 1924;Diogo et al 2016;Molnar et al 2018). The evolution and resulting homologies of the skeletal elements of the pectoral girdle and forelimbs are comparably well known and supported by the fossil record (e.g., McGonnell 2001;Coates et al 2002;Shubin et al 2006Shubin et al , 2009Ponomartsev et al 2017), whereas the related soft tissues have rarely been considered (Soliz et al 2018; but see, e.g., Rolleston 1869, Romer 1922, and Abdala and Diogo 2010 for attempts to assess forelimb muscle homologies across tetrapods and Diogo et al 2016 andMolnar et al 2018 for the reconstruction of muscle evolution across the fin-to-limb transition).…”