A timeline of pharyngeal endoskeletal condensation and differentiation in the shark, Scyliorhinus canicula, and the paddlefish, Polyodon spathula

Abstract

The lesser-spotted dogfish (Scyliorhinus canicula) and the North American paddlefish (Polyodon spathula) are two emerging model systems for the study of vertebrate craniofacial development. Notably, both of these taxa have retained plesiomorphic aspects of pharyngeal endoskeletal organization, relative to more commonly used models of vertebrate craniofacial development (e.g. zebrafish, chick and mouse), and are therefore well suited to inform the pharyngeal endoskeletal patterning mechanisms that functioned in the last common ancestor of jawed vertebrates. Here, we present a histological overview of the condensation and chondrogenesis of the most prominent endoskeletal elements of the jaw, hyoid and gill arches - the palatoquadrate/Meckel's cartilage, the hyomandibula/ceratohyal, and the epi-/ceratobranchial cartilages, respectively - in embryonic series of S. canicula and P. spathula. Our observations provide a provisional timeline and anatomical framework for further molecular developmental and functional investigations of pharyngeal endoskeletal differentiation and patterning in these phylogenetically informative taxa.

Figure 1

Schematic overview of pharyngeal endoskeletal organization in a shark, paddlefish, zebrafish and mouse. In all images, anterior is to the left. Mandibular arch derivatives are colored in red, hyoid arch derivatives are colored in blue and gill arch derivatives are colored in yellow. The paddlefish schematic was drawn from an original specimen (derivatives of gill arch 4 and 5 are obscured); the shark schematic was redrawn from a specimen figured in Gillis et al. (2011) (note that branchial rays are not shown); the zebrafish schematic was redrawn from a 6 day-post-fertilization specimen figured in Schilling et al. (1996); the mouse schematic was redrawn from Depew et al. (2005). Abbreviations: at, ala temporalis; bh, body of the hyoid; cb1-5, ceratobranchials 1-5; ch, ceratohyal; eb1-4, epibranchials 1-4; ghh, greater horn of the hyoid; hm, hyomandibula; hs, hyosymplectic; in, incus; lc, laryngeal cartilages; lhh, lesser horn of the hyoid; ma, malleus; mk, Meckel’s cartilage; mk^rp, rostral projection of Meckel’s cartilage; pq, palatoquadrate; sp, styloid process; st, stapes; thy, thyroid cartilage.

Figure 2

Horizontal histological sections through the mandibular (MA), hyoid (HA) and gill arches 1-5 (GA1-5) of the lesser-spotted dogfish, Scyliorhinus canicula, at (a-g) stage (St.) 26, (h-n) St. 28, (o-u) St. 29/30 and (v-bi) St. 31. In all images, anterior is to the left. For histological details, see text. Abbreviations: br, branchial ray; cb1-5, ceratobranchial 1-5; hm, hyomandibula; mk, Meckel’s cartilage. * indicates an as-yet undifferentiated mesenchymal condensation. All scale bars = 20μm.

Figure 3

Horizontal histological sections through the mandibular (MA), hyoid (HA) and gill arches 1-5 (GA1-5) of the North American paddlefish, Polyodon spathula, at (a-e) stage (St.) 36, (f-j) St. 40, (k-o) st. 44 and (p-t) St. 46. In all images, anterior is to the left. For histological details, see text. Abbreviations: cb1-5, ceratobranchial 1-5; hm, hyomandibula; pq, palatoquadrate. * indicates an as-yet undifferentiated mesenchymal condensation. All scale bars = 20μm.