Early Palaeozoic dentine and patterned scales in the embryonic catshark tail

Abstract

Regular scale patterning, restricted to the caudalmost tail and organized into two opposing rows on each side of the tail, is observed in few chondrichthyans. These evenly spaced scales, in dorsal and ventral rows, develop in an iterative sequence from the caudal tip, either side of the notochord. They are subsequently lost as a scattered pattern of placoid scales develops on the body and fins. An identical organized pattern is observed in tail scales of Scyliorhinus canicula (catshark), where the expression of sonic hedgehog signal is restricted to the epithelium of developing scales and remains localized to the scale pocket. Regulation of iterative scale position by sonic hedgehog is deeply conserved in vertebrate phylogeny. These scales also reveal an archaic histological structure of a dentine type found in the oldest known shark scales from the Ordovician and Silurian. This combination of regulated pattern and ancient dentine occurs only in the tail, representing the primary scalation. Scattered body scales in elasmobranchs such as S. canicula originate secondarily from differently regulated development, one with typical orthodentine around a central pulp cavity. These observations emphasize the modular nature of chondrichthyan scale development and illustrate previously undetected variation as an atavism in extant chondrichthyan dentine.

Figure 1

SEM images showing S. canicula tail tip, with arrangement of two offset rows of scales. (a–c) Stage 31: (a) left lateral view, (b) newest round-topped scales (arrows), (c) caudalmost tail tip, terminal scale absent. (d–g) Stage 33: (d) left lateral view, one more scale on dorsal row (arrows indicate scales in (e)). (f,g) Older, lozenge-shaped scales, scale pocket epithelium (asterisk). Scale bars, (a) 0.50 mm, (b) 86 μm, (c) 176 μm, (d,f,g) 0.60 mm and (e) 120 μm. (a,d) Arrowheads indicate rostral.

Figure 2

Scale rows at S. canicula tail tip showing arrangement and histology compared to Ordovician scales from the Harding Sandstone. (a–d) Tail tip in left lateral view. (a) Transmitted light showing iterative scale pockets at stage 29 with an rostrocaudal stagger 9/10 dorsal and 8/9 ventral. (b) Incident light reflected from erupted scale surfaces showing tail shape (stage 33). (c) Photomacrograph (stage 32) and (d) Nomarski optics (DIC; stage 33) of whole mount in situ hybridization for Scshh showing expression patterns as iterative focal loci restricted to scale positions. (e–j) Scale histology in H&E stained vertical sections through the four scale rows (stage 33, DIC). (h) Scales either side of neural tube and notochord with large flat crowns and slender necks, (i) similar but ventral tail end (arrow, scale in (e)). (e) Mature scale showing two dentine canals and odontoblast cells below extended neck. (f) Young scale with shorter neck and odontoblast cell bodies in the dentine below the tubules. (g) More rostral, younger scale in (j) from dorsal row next to neural tube, with open base, several wide canals and odontoblast cell bodies below these. (k,l) Mineralized ground sections (DIC) of Ordovician shark microremains from Colorado (see also Sansom et al. 1996, fig. 1). (k) Higher magnification of crown dentine (line in (l)) of whole scale, mineral deposits in the spaces show tubular dentine with multiple branching from a wide central canal extending down through the extensive scale base. Abbreviations, d.can, dentine canal; d.tub, dentine tubule; od, odontoblasts. Scale bar, (a,c) 20 mm, (b) 500 μm, (d) 100 μm, (e–h) 10 μm and (i–l) 50 μm.