Development of dermal denticles in skates (Chondrichthyes, Batoidea): Patterning and cellular differentiation

Abstract

Patterning, cellular differentiation, and developmental sequences of dermal denticles (denticles) are described for the skate Leucoraja erinacea. Development of denticles proceeds caudo-rostrally in the tail and trunk. Once three rows of denticles form in the tail and trunk, denticles begin to appear in the region of the pelvic girdle, medio-caudal to the eyes and on the pectoral fins. Although timing of cellular differentiation of denticles differs among different locations of the body, cellular development of a denticle is identical in all locations. Thickening of the epidermis as a denticle lamina marks initiation of development. A single lamina for each denticle forms, and a small group of mesenchymal cells aggregates underneath it. The lamina then invaginates caudo-rostrally to form the inner- and outer-denticle epithelia (IDE and ODE, respectively). Before nuclei of IDE cells are polarized, enameloid matrix appears between the basement membrane of the IDE and the apical surface of the pre-odontoblasts. Pre-dentin is then laid down along with collagenous materials. Von Kossa stain visualizes initial mineralization of dentin, but not enameloid. During the growth of a denticle, dense fibrous connective tissue of the dermis forms the deep dermal tissue over the dorsal musculature. Attachment fibers and tendons anchor denticles and dorsal musculature, respectively, on deep dermal tissue. Basal tissue of the denticles develops as the denticle crown grows. If the basal tissue is bone of attachment, then the cells along the basal tissue would be osteoblasts. However, these cells could not be distinguished from odontoblasts using immunolocalization of type I pro-collagen (Col I), alkaline phosphatase (APase), and neural cell adhesion molecule (N-CAM). Well-developed dentin, (not pre-dentin), the enameloid matrix (probably when it begins to mineralize), and deep dermal tissue are Verhoeff stain-positive, suggesting that these tissues contain elastin and/or elastin-like molecules. Our study demonstrates that the cellular development of denticles resembles tooth development in elasmobranchs, but that dermal denticles differ from teeth in forming from a single denticle lamina. Whether the basal tissue of denticles is bone of attachment remains undetermined. Confirmation and function of Verhoeff-positive proteins in enameloid, dentin, and deep dermal tissue remain to be determined. We discuss these issues along with an analysis of recent findings of enamel and enameloid matrices.

Early Palaeozoic dentine and patterned scales in the embryonic catshark tail

“…We suggest that the 'patterned tail scale' module represents the more ancient, relative to the scattered body scales, which may be related to suggestions that the tail is itself an independent developmental unit relative to the rest of the body (reviewed in Handrigan 2003). Data on pattern regulation and histology of tail scales in other taxa, and the histology of bilaterally axially patterned scales on the body during early ontogeny, for example, in holocephalans (Didier 2004) and other elasmobranchs (Miyake et al 1999;Freitas & Cohn 2004) would test these hypotheses.…”

“…Miyake et al 1999;Didier 2004;Freitas & Cohn 2004;Eames et al 2007). This patterning is observed in bilateral scale rows along the body and rows associated with the lateral sensory canals; patterned scale rows have also been described in association with the tail fin (axial lobe).…”

The genetic basis of modularity in the development and evolution of the vertebrate dentition

“…As demonstrated by Miyake et al (1999), elasmobranchs (sharks, skates and rays) provide a promising system for comparing gene expression between dermal denticles, true teeth and oropharyngeal denticles. Another group of organisms with potential in this respect are ¢shes of the genus Polypterus, which possess odontodes on dermal bones, scales, ¢n spines and throughout the oropharyngeal region (Meinke 1982;Jollie 1984).…”

Dermal denticle patterning in the Cretaceous hybodont sharkTribodus limae(Euselachii, Hybodontiformes), and its implications for the evolution of patterning in the chondrichthyan dermal skeleton

“…Despite the seemingly disorganized distribution of denticles in the skin of most adult elasmobranchs, the ontogenetically earliest denticles may be arranged in distinct rows at specific sites: on either side of the caudal fin axis in Heterodontus (Johanson et al, 2007), from the pectoral fins to the caudal peduncle in Scyliorhinus (Freitas and Cohn, 2004), and along both sides of the caudal peduncle in Cephaloscyllium and Squalus (Grover, 1974;Maisey, 1974). Thus, initial denticle patterning in elasmobranchs can be highly organized, but this transient stage can disappear secondarily; in skates, however, some of the first denticles to form in juveniles are arranged in rostrocaudal rows that are retained into adulthood (Grover, 1974;Miyake et al, 1999). It has been suggested that initial denticle patterning in Heterodontus is related to myomere pattern (Johanson et al, 2007), as with osteichthyan scales (Sire and Akimento, 2004).…”

“…However, unlike pigmentation patterns, which are related to the differential distribution of melanocyte cells, dermal denticles form de novo at the interface of the epidermis and dermis, on the basal lamina (e.g., Miyake et al, 1999;Barrio et al, 2009). Reaction-diffusion models that involve coupling between layers (Yang et al, 2002;Barrio et al, 2009;Madzvamuse et al, 2015) approximate the interaction of morphogens through the basal lamina between the epidermal and dermal layers.…”