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.
Highlights
A dermal skeleton composed of odontodes, discrete dentine structures that develop around a mesenchymal papilla in contact with an overlying epithelium, is primitively present both on the external body surface and in the oro-pharynx of jawed vertebrates
The presence of a similar odontode pattern in fossils has been inferred to indicate the existence of a dental lamina or odontogenic band during their development [3,12]
What these two growth modes mean in a 3D context cannot be addressed based only on 2D thin sections, and the true morphology of each odontode cannot be inferred from the surface of the scale
Summary
A dermal skeleton composed of odontodes, discrete dentine structures (sometimes covered with enamel or enameloid) that develop around a mesenchymal papilla in contact with an overlying epithelium, is primitively present both on the external body surface and in the oro-pharynx of jawed vertebrates. One major exception to this rule is the Chondrichthyes (sharks, rays and ratfishes), which frequently have well-developed dermal odontode skeletons composed of placoid scales (Figure 1), as well as teeth in the jaws. The other major groups of jawed vertebrates, ‘Acanthodii’, ‘Placodermi’ (both probably paraphyletic [15]) and Osteichthyes, all primitively have polyodontode scales (Figure 1), meaning that each scale is formed from multiple odontodes attached to a bony base. Such a scale grows larger and thicker during the life span of the fish and is not shed. Our results challenge the hypothesis of a rigid distinction between external and oro-pharyngeal odontode patterning
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