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

Date Published: September 4, 2013

Publisher: Public Library of Science

Author(s): Aaron R. H. LeBlanc, Robert R. Reisz, Laurent Viriot.


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.

Partial Text

Tooth implantation is an important criterion for interpreting evolutionary events in major groups of tetrapods. The geometry of the attachment site of the tooth to the jaw has been used in phylogenetic reconstructions of lissamphibians [1], snakes and other squamates [2], [3] and mammals [4]. In general, three types of implantation are recognized: acrodonty (a tooth is attached to the apex of the jaw), pleurodonty (a tooth is attached to the lingual surface of the jaw), and thecodonty (a tooth is set into a deep socket in the jaw). Although these categories are convenient for partitioning tooth implantation into discrete types, or even character states, these three arrangements do not encompass the total diversity of ways in which teeth are implanted and attached to the jaws of tetrapods [4]. Some authors have proposed additional categories that take into account the geometry of implantation, as well as the nature of attachment of the tooth to the jaw in order to provide more specific classifications [4]. These classifications, however, have led to ambiguous and often conflicting interpretations of tooth implantation, particularly in extinct taxa [5], [6]. A more detailed and consistent definition of tooth implantation categories can be formulated at the histological level, which can be done for both extinct and extant groups [2], [7], [8].

Permission was obtained from all of the relevant institutions (Texas Memorial Museum in Austin, Texas; the Harvard University Museum of Comparative Zoology in Cambridge, Massachusetts; Royal Ontario Museum in Toronto, Canada) to access and work on the specimens that have been borrowed from their collections. All specimens were loaned to R. R. Reisz with permission for preparation and thin-sectioning.

Taphonomic and diagenetic processes can alter tissues of animals. We therefore propose to use a fossil horse specimen (Equus sp., ROM 33036) from the Pleistocene of Florida, USA for comparisons with the tissues observed in diadectids in order to ensure consistent definitions of the individual tooth and periodontal tissues across fossil taxa, using the mammalian condition as a reference. This approach allows us to understand how the mammalian condition for tooth implantation and attachment is modified after fossilization, and therefore reconstruct the tissues that originally existed in the diadectid jaw, before fossilization. All periodontal tissues that are present in extant horses are readily identifiable in cross-sections of ROM 33036, including the mineralized portion of the periodontal ligament (Figure 3). As hypsodont (high-crowned) ungulates, horses possess highly infolded and extensive layers of dentine, enamel, and cementum that form significant portions of the tooth [28]. The enamel, typically associated with the portion of the crown that is above the jawbone and gum line in brachydont (short-crowned) mammals, is found in cross-sections that are taken from deep within the jaw in Equus sp. (Figure 3A, 3B). Layers of cellular cementum coat the periphery of the tooth and are external to the enamel. Normally this tissue is situated external to the dentine of the tooth root in brachydont mammals [29]. Under cross-polarized light, the cellular cementum contains numerous Sharpey’s fibers, which extend radially around the tooth (Figure 3B). These Sharpey’s fibers mark the insertion points for the periodontal ligament into the cellular cementum. The unmineralized portion of the periodontal ligament would have occupied the area external to the cellular cementum. In its place is a void in fossilized specimens, which is partially or completely infilled with diagenetic minerals in different parts of the alveoli in the Equus sp. material (Fig. 3A, 3B). Alveolar bone forms the inner walls of the tooth socket (Figure 3B, 3C). This tissue is separated from the bone of the jaw by a reversal line in some areas, which indicates the farthest extent to which bone of the jaw had been resorbed to accommodate the alveolar bone (Figure 3C). Alveolar bone in Equus sp. is highly remodeled and highly vascularized. Secondary osteons are prevalent throughout the alveolar bone, but are particularly abundant in more external layers (those closest to the bone of the jaw). Primary bone tissues are confined to the regions that are closest to the periodontal space. These internal layers are composed of lamellar bone with abundant Sharpey’s fibers (Figure 3B). This tissue, termed bundle bone, provides anchorage for the periodontal ligament into the walls of the alveolus [29].

Comparisons between diadectid, mammalian and crocodilian forms of thecodonty demonstrate that teeth of these three taxa were implanted and attached in similar fashions. We reject the hypothesis that tooth attachment in diadectids was through ankylosis to “bone of attachment” and emphasize that the attachment of the tooth root to the socket in diadectids is much more complex than previously thought. The tooth root is coated in successive layers of acellular and cellular cementum, which were connected to alveolar bone by a ligamentous attachment (a thecodont gomphosis) that mineralized later in ontogeny of the tooth or of the animal (Figure 10). Very little remains of the periodontal ligament in diadectids, because any soft tissue components of the periodontium would have been lost shortly after death of the animal, as was demonstrated in the thin sections of a fossil horse (Figure 3). However, dense networks of Sharpey’s fibers within the alveolar bone and cementum in the diadectid specimens could only have formed as the mineralized components of a ligament within the alveolus: the periodontal ligament. Furthermore, edentulous upper and lower jaws of diadectids provide taphonomic evidence that a soft tissue attachment between the tooth roots and the alveoli must have existed at a particular point in the lifespan of each tooth. Any form of ankylosis that occurred in diadectids was thus through mineralization of the periodontal ligament and not through fusion of the tooth root to “bone of attachment”, more properly called alveolar bone.