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. 2013 Sep 4;8(9):e74697.
doi: 10.1371/journal.pone.0074697. eCollection 2013.

Periodontal Ligament, Cementum, and Alveolar Bone in the Oldest Herbivorous Tetrapods, and Their Evolutionary Significance

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Periodontal Ligament, Cementum, and Alveolar Bone in the Oldest Herbivorous Tetrapods, and Their Evolutionary Significance

Aaron R H LeBlanc et al. PLoS One. .
Free PMC article

Abstract

Tooth implantation provides important phylogenetic and functional information about the dentitions of amniotes. Traditionally, only mammals and crocodilians have been considered truly thecodont, because their tooth roots are coated in layers of cementum for anchorage of the periodontal ligament, which is in turn attached to the bone lining the alveolus, the alveolar bone. The histological properties and developmental origins of these three periodontal tissues have been studied extensively in mammals and crocodilians, but the identities of the periodontal tissues in other amniotes remain poorly studied. Early work on dental histology of basal amniotes concluded that most possess a simplified tooth attachment in which the tooth root is ankylosed to a pedestal composed of "bone of attachment", which is in turn fused to the jaw. More recent studies have concluded that stereotypically thecodont tissues are also present in non-mammalian, non-crocodilian amniotes, but these studies were limited to crown groups or secondarily aquatic reptiles. As the sister group to Amniota, and the first tetrapods to exhibit dental occlusion, diadectids are the ideal candidates for studies of dental evolution among terrestrial vertebrates because they can be used to test hypotheses of development and homology in deep time. Our study of Permo-Carboniferous diadectid tetrapod teeth and dental tissues reveal the presence of two types of cementum, periodontal ligament, and alveolar bone, and therefore the earliest record of true thecodonty in a tetrapod. These discoveries in a stem amniote allow us to hypothesize that the ability to produce the tissues that characterize thecodonty in mammals and crocodilians is very ancient and plesiomorphic for Amniota. Consequently, all other forms of tooth implantation in crown amniotes are derived arrangements of one or more of these periodontal tissues and not simply ankylosis of teeth to the jaw by plesiomorphically retaining "bone of attachment", as previously suggested.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Comparisons of the tooth tissues in a generalized thecodont and subthecodont condition.
A: thecodont tooth implantation in labiolingual section. B: subthecodont tooth implantation in labiolingual section. ab, alveolar bone; ac, acellular cementum; boa, bone of attachment; cc, cellular cementum; de, dentine; en, enamel; jb, jawbone; pc, pulp cavity; pdl, periodontal ligament; po, primary osteon; sf, Sharpey's fibers; so, secondary osteon; vc, vascular canal.
Figure 2
Figure 2. Phylogenetic position of Diadectomorpha and reconstruction of a diadectid skull.
A: cladogram of stem and crown amniotes that are discussed. Modified from Maxwell, Caldwell, and Lamoureux . Bolded terminal taxa are those that have representatives that possess alveolar bone and cementum. B: reconstruction of a diadectid skull in lateral view. Modified from Reisz . Note the presence of anterior incisiform and posterior molariform teeth. C: reconstruction of a diadectid skull in ventral view. Modified from Reisz . inc, incisiform teeth; mol, molariform teeth.
Figure 3
Figure 3. Dental histology of Equus sp. (ROM 33036).
A: overview image of a cross-section through the partial left mandible of ROM 33036, taken parallel to the tooth row and bisecting a molariform tooth. B: closeup of the periodontal region in A under cross-polarized light. Note the presence of Sharpey's fibers on either side of the periodontal space, indicating the presence of a periodontal ligament that has since disintegrated. C: closeup of the alveolar bone in A under cross-polarized light. Arrows highlight the position of a reversal line between the alveolar bone and the jawbone. ab, alveolar bone; bb, bundle bone layer within the alveolar bone; cc, cellular cementum; de, dentine; en, enamel; jb, jawbone; ps, periodontal space; sf, Sharpey's fibers.
Figure 4
Figure 4. Dental histology of a molariform tooth in Diadectes sp. (MCZ 7874) from the Permian of Texas.
A: overview image of a labiolingual section of a molariform tooth from an isolated dentary. The red boxes correspond to the positions of images C–F. B: interpretation of the dental tissues in A. The alveolar bone is shaded grey. The red boxes correspond to the positions of images C–F. C: closeup of the tooth root from the labiolingual section in A. D: closeup of the tooth root and adjacent alveolar bone from the labiolingual section in A. Note the absence of a periodontal space between the alveolar bone and the tooth root. E: closeup of the alveolar bone and the adjacent jawbone from the labiolingual section in A. Note the darker color of the alveolar bone, which is a result of a high density of Sharpey's fibers. F: same image as in E, but under cross-polarized light. Note the reversal line highlighted by the black arrows, which separates the woven bone of the alveolus from the Haversian bone of the jaw. ab, alveolar bone; ac, acellular cementum; de, dentine; dl, dentine lamellae; gzd, globular zone of dentine; jb, jawbone; po, primary osteon; sf, Sharpey's fibers.
Figure 5
Figure 5. Cross-sectional views of the molariform teeth of Diadectes sp. from the Permian of Texas.
A: overview image of a cross-section through the roots of three molariform teeth of Diadectes sp. (MCZ 7871). Note the presence of large resorption pits lingual to the tooth roots, which have invaded the pulp cavities of two of the teeth. Red box indicates position of image E. B: Interpretation of the dental tissues in A. Grey areas indicate alveolar bone of each associated root, with darker shades of grey indicating older generations of alveolar bone. Dashed lines indicate reversal lines. C: cross-section of a large diadectid molariform tooth root (TMM 43628-3), possessing thick layers of cementum and clear dentine infoldings. D: same image as in C, but under cross-polarized light. Note the distinct boundary between the acellular cementum and the dentine, and the extension of the acellular cementum into the cores of some of the dentine infoldings. Also note the presence of Sharpey's fibers in the cellular cementum. E: closeup of a Diadectes tooth root and alveolar bone from image A. F: same image as E, but under cross-polarized light. Note the presence of acellular cementum within the cores of some of the dentine infoldings and the birefringence of the cellular cementum layer. ab, alveolar bone; ac, acellular cementum; cc, cellular cementum; dd, dark dentine; de, dentine; dl, dentine lamella; gzd, globular zone of dentine; jb, jawbone; pc, pulp cavity; po, primary osteon; rl, reversal line; rp, resorption pit; sf, Sharpey's fibers.
Figure 6
Figure 6. Longitudinal section of the incisiform teeth of a diadectid (TMM 43628-3) from the Lower Permian of Texas.
A: Overview image of a longitudinal section through two complete tooth roots. Red boxes correspond to images C–F. B: interpretation of the arrangements of the periodontal tissues of diadectids in longitudinal section. Grey areas indicate alveolar bone and darker areas indicate the presence of older generations of alveolar bone from previous teeth. Red boxes correspond to the positions from which images C–F were taken. C: closeup of the root of one of the teeth from image A. Note the presence of acellular and cellular cementum, as well as an apparent periodontal space. D: closeup of of the tooth root and socket of one of the teeth from image A. The darker coloration of the alveolar bone is due to the presence of Sharpey's fibers. Note the presence of another bone tissue forming the wall of the alveolus, here referred to as the interdental plate. E: closeup of the base of a tooth root and alveolar bone from image A. F: closeup of the base of the alveolus of one of the teeth from image A. Note the presence of multiple generations of alveolar bone forming the floor of the alveolus. ab, alveolar bone; ac, acellular cementum; cc, cellular cementum; de, dentine; idp, interdental plate; jb, jawbone; oab, old generation of alveolar bone; pc, pulp cavity; rl, reversal line; sf, Sharpey's fibers; so, secondary osteons.
Figure 7
Figure 7. Comparisons of the periodontal tissues between diadectids and a fossil horse.
A: longitudinal section of cellular cementum in a molariform tooth of Equus sp. (ROM 33036) under normal light. B: longitudinal section of the acellular and cellular cementum of a diadectid molariform tooth (TMM 43628-3). Image was taken using an oblique illumination slider to highlight the incremental growth lines in the cellular cementum. C: longitudinal section of cellular cementum in Equus sp. (ROM 33036) under cross-polarized light. Note the extensive network of parallel Sharpey's fibers that mark the insertions of the periodontal ligament. D: closeup of the acellular and cellular cementum of a diadectid tooth (TMM 43628-3). Note the presence of a network of parallel Sharpey's fibers that mark the insertions of the periodontal ligament. E: closeup of the alveolar bone of Equus sp. (ROM 33036) in cross-section. Note the presence of Sharpey's fibers in the alveolar bone layers that border the periodontal space. F: closeup of the alveolar bone of a diadectid (TMM 43628-3) in cross-section. Note the presence of dense networks of Sharpey's fibers in successive layers of alveolar bone. A reversal line separates each layer of alveolar bone. ab, alveolar bone; ac, acellular cementum; bb, bundle bone layer of the alveolar bone; cc, cellular cementum; cl, cementocyte lacunae; igl, incremental growth lines in the cementum; ps, periodontal space; rl, reversal line; sf, Sharpey's fibers.
Figure 8
Figure 8. Taphonomic evidence for the presence of periodontal ligaments in diadectids and crocodilians.
A: ventral view of a complete right upper jaw (premaxilla and maxilla) of a diadectid (TMM 43628-2) that exhibits post-mortem tooth loss. Nearly all of the teeth are interpreted as having been lost after the periodontal ligament had decomposed. B: dorsal view of a dentary of a modern Alligator mississippiensis (ROM 690) that exhibits post-mortem tooth loss. All of the teeth have fallen out as a result of a loss of the periodontal ligament after death. C: an isolated diadectid tooth with a complete root from the Lower Permian Dolese Brothers Quarry near Richards Spur, Oklahoma, part of a collection of isolated diadectid teeth from the Sam Noble Oklahoma Museum of Natural History in Normal, Oklahoma (OMNH 56872). The presence of a complete root and a worn crown suggest that this tooth was functional and was not shed from the jaw, but was lost post-mortem. Note the presence of a thick layer of cementum coating the root. D: an isolated tooth of Alligator mississippiensis (ROM 690) that has fallen out of the dentary due to the loss of the periodontal ligament.
Figure 9
Figure 9. Longitudinal section of an isolated diadectid incisiform tooth (ROM 65911).
ac, acellular cementum; cc, cellular cementum; cl, cementocyte lacunae; de, dentine; gzd, globular zone of dentine.
Figure 10
Figure 10. Interpretation of the development of the periodontal tissues in diadectids in a full tooth replacement cycle.
A: the periodontal tissues of an incisiform tooth are fully developed; the tooth is bounded to the alveolus by a completely mineralized periodontal ligament and alveolar bone. B: a replacement tooth begins to form within a resorption pit lingual to the functional tooth, causing resorption of the surrounding dentine and periodontal tissues. C: the replacement tooth and resorption pit enlarge, invading the pulp cavity of the functional tooth. D: the functional tooth is shed and the replacement tooth begins to migrate into the oral cavity. Not all of the alveolar bone from the previous generation is resorbed. Root dentine and acellular cementum of the replacement tooth begin to form. E: The new tooth becomes functional and is suspended by an unmineralized periodontal ligament. The tooth root is coated in both acellular and cellular cementum. A new generation of alveolar bone overlies the previous layer. F: the fully mature tooth is firmly attached to the alveolus by a mineralized periodontal ligament. ab, alveolar bone; ac, acellular cementum; cc, cellular cementum; de, dentine; jb, jawbone; mpdl; mineralized periodontal ligament; oab, older generation of alveolar bone; pc, pulp cavity; pdl, periodontal ligament; rl, reversal line; rp, resorption pit; rt, replacement tooth; sf, Sharpey's fibers.

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Grant support

ARHL was supported by an NSERC Postgraduate Student doctoral scholarship. RRR was supported by a Discovery Grant from NSERC. The funders had no role in study design, data collection and analysis, decisions to publish, or preparation of the manuscript.
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