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.

From body scale ontogeny to species ontogeny: Histological and morphological assessment of the Late Devonian acanthodian Triazeugacanthus affinis from Miguasha, Canada

“…The first hypothesis suggests a role of Shh and/or ScShh which is known to be involved in the positional specification along the antero-posterior axis in vertebrates [114, 121]. Shh expression is involved in the control of epidermal-dermal interactions but seems not essential for scale initiation and patterning of squamation [104].…”

Evolution of developmental pattern for vertebrate dentitions: an oro‐pharyngeal specific mechanism

“…It appears that a regular pattern was not present in the early stages of denticle formation in the shark skin but that close spacing only developed with time, as Reif ('82) recorded that the first generation of skin denticles (placoid scales) is very widely spaced and with variable positions. In contrast to this lack of order in the skin, it is known that much earlier than the development of any body denticles, a set do form in a sequential, regular time and space order on the embryonic tail in at least some sharks, even though they are lost by shedding soon after hatching (Johanson et al, 2007, 2008). Denticles are rarely shed from the body skin, so that the cover arises slowly with growth as more and more individual denticles are added.…”

“…One explanation for control of new sites of denticle formation is the “nearest neighbor hypothesis” (Reif, '85; Johanson et al, 2008), likely making use of local genetic and cellular components. Possibly there is a requirement to be near other denticles to initiate denticle formation from putative stem cell‐like populations.…”

“…It may be so, in earlier evolutionary time that no pattern was available to be co‐opted from the skin to the mouth to function as tooth sets. It is noteworthy that earlier in embryology the tail pattern of denticles is very ordered but from caudal to rostral and it may be an older and alternative mechanism that is replaced in evolution by the secondary and later developing body pattern (Johanson et al, 2008). …”

“…Currently there is active discussion and debate over the theories that might explain how the system for dentitions evolved from skin denticle systems, especially at the jaw margins. In order to assess the relationship between dental and skin denticle patterns, we present data on patterns of skin denticles in the catshark ( Scyliorhinus canicula ) and emphasize that, although almost nothing is known about molecular regulation of patterning in the skin (Johanson et al, 2007, 2008), at least from the structural pattern for spacing and replacement there is no obvious organization of these denticles that could be suitably co‐opted and converted into a pattern that might have evolved into “tooth sets.”…”