Scales and Tooth Whorls of Ancient Fishes Challenge Distinction between External and Oral ‘Teeth’

Abstract

The debate about the origin of the vertebrate dentition has been given fresh fuel by new fossil discoveries and developmental studies of extant animals. Odontodes (teeth or tooth-like structures) can be found in two distinct regions, the ‘internal’ oropharyngeal cavity and the ‘external’ skin. A recent hypothesis argues that regularly patterned odontodes is a specific oropharyngeal feature, whereas odontodes in the external skeleton lack this organization. However, this argument relies on the skeletal system of modern chondrichthyans (sharks and their relatives), which differ from other gnathostome (jawed vertebrate) groups in not having dermal bones associated with the odontodes. Their external skeleton is also composed of monoodontode 'placoid scales', whereas the scales of most early fossil gnathostomes are polyodontode, i.e. constructed from several odontodes on a shared bony base. Propagation phase contrast X-ray Synchrotron microtomography (PPC-SRµCT) is used to study the polyodontode scales of the early bony fish Andreolepis hedei. The odontodes constructing a single scale are reconstructed in 3D, and a linear and regular growth mechanism similar to that in a gnathostome dentition is confirmed, together with a second, gap-filling growth mechanism. Acanthodian tooth whorls are described, which show that ossification of the whorl base preceded and probably patterned the development of the dental lamina, in contrast to the condition in sharks where the dental lamina develops early and patterns the dentition.The new findings reveal, for the first time, how polyodontode scales grow in 3D in an extinct bony fish. They show that dentition-like odontode patterning occurs on scales and that the primary patterning unit of a tooth whorl may be the bony base rather than the odontodes it carries. These results contradict the hypothesis that oropharyngeal and external odontode skeletons are fundamentally separate and suggest that the importance of dermal bone interactions to odontode patterning has been underestimated.

The origin of novel features by changes in developmental mechanisms: ontogeny and three‐dimensional microanatomy of polyodontode scales of two early osteichthyans

“…For example, the lines of arrested growth (LAGs) in bone can be used to identify the age and developmental stage of organisms (Francillon-Vieillot et al, 1990;Castanet et al, 1993). The sequence of buried denticles or odontodes in the dermal skeleton of many Palaeozoic vertebrates can also be informative about the developmental stage of the dermal skeleton (Ørvig, 1978a,b,c;Qu et al, 2013a). However, thin sections can only provide partial information about such 3D ontogenetic sequences.…”

“…This imaging method has been applied successfully to both living and fossils organisms to show the 3D microstructure of hard tissues in situ (e.g. Rücklin et al, 2012;Sanchez et al, 2012Sanchez et al, , 2013Qu et al, 2013aQu et al, , 2015a. The high-resolution PPC-SRμCT scans can produce high-quality virtual thin sections that are comparable to classical thin sections (except for the orientation and organisation of the apatite crystals within the bone matrix), with submicron structures such as osteocytes and dentine tubules being visible, while also recording the complete 3D distribution pattern of the microstructures (e.g.…”

“…The high-resolution PPC-SRμCT scans can produce high-quality virtual thin sections that are comparable to classical thin sections (except for the orientation and organisation of the apatite crystals within the bone matrix), with submicron structures such as osteocytes and dentine tubules being visible, while also recording the complete 3D distribution pattern of the microstructures (e.g. Sanchez et al, 2012Sanchez et al, , 2013Sanchez et al, , 2014Giles, Rücklin & Donoghue, 2013;Qu et al, 2013a). In addition, the 3D data make it possible to examine how the dermal skeletal elements of extinct vertebrates developed in space and time (e.g.…”

Morphology and histology of acanthodian fin spines from the late Silurian Ramsåsa E locality, Skåne, Swede

“…Furthermore, the use of propagation phase-contrast synchrotron X-Ray microtomography technology as a nondestructive tool for studying the 3D microstructure of fossils has made it possible to understand aspects of their overall architecture that might not be observed from traditional 2D thin section (e.g., Sanchez et al, 2012;Qu et al, 2015). This technique has been used to study the histology of a number of fossils, including scales (e.g., Qu et al, 2013Qu et al, , 2015, dermal plates (e.g., Dupret et al, 2010;Giles et al, 2013;Chen et al, 2016), fin bones and rays (Sanchez et al, 2014), and fin spines , and has provided valuable information on the morphology, vascularization, and growth of these structures.…”

Histological Observation of the Jaws and Teeth of the Green Spotted Pufferfish<i> (Tetraodon Nigroviridis)</i>

“…The dermal tooth (placoid scale) covering the body surface of sharks, cartilaginous fish, is considered to be the origin of the teeth of mammals including humans 1) , and many reports on the evolutionary process connecting sharks and humans have been published [2][3][4][5][6] . The crown surface of mammalian teeth contains epithelial enamel, whereas the teeth of most fish contain enameloid, which is structurally different from enamel, and studies to investigate fish teeth to clarify the evolution of enamel are considered necessary [7][8][9][10] .…”