Tooth attachment and pleurodont implantation in lizards: Histology, development, and evolution

Abstract

Squamates present a unique challenge to the homology and evolution of tooth attachment tissues. Their stereotypically pleurodont teeth are fused in place by a single "bone of attachment", with seemingly dubious homology to the three-part tooth attachment system of mammals and crocodilians. Despite extensive debate over the interpretations of squamate pleurodonty, its phylogenetic significance, and the growing evidence from fossil amniotes for the homology of tooth attachment tissues, few studies have defined pleurodonty on histological grounds. Using a sample of extant squamate teeth that we organize into three broad categories of implantation, we investigate the histological and developmental properties of their dental tissues in multiple planes of section. We use these data to demonstrate the specific soft-and hard-tissue features of squamate teeth that produce their disparate tooth implantation modes. In addition, we describe cementum, periodontal ligaments, and alveolar bone in pleurodont squamates, dental tissues that were historically thought to be restricted to extant mammals and crocodilians. Moreover, we show how the differences between pleurodonty and thecodonty do not relate to the identity of the tooth attachment tissues, but rather the arrangements of homologous tissues around the teeth.

Dental ontogeny in extinct synapsids reveals a complex evolutionary history of the mammalian tooth attachment system

“…Heterochrony has played a prominent role in the diversification of mammalian teeth, including evolutionary changes to eruption timing and the evolution of high-crowned (hypsodont) teeth [49,50], but it has played a further role in the evolution of the dental gomphosis that characterizes all mammal teeth. Evolutionary changes to the timing of calcification of the tooth attachment tissues were not restricted to synapsids, however, as similar phenomena have been proposed to explain the occurrences of a ligamentous tooth attachment in some extant and extinct squamates [23]. These similarities between synapsid and squamate dental ontogeny and evolution suggest that heterochrony may be an important driver of dental attachment tissue evolution in amniotes.…”

“…R. Soc. B 285: 20181792 Sharpey's fibres and a sediment-or mineral-filled gap between the tooth root and the socket bone are therefore strong indicators of the presence of a PDL in a fossil vertebrate [20,23,28].…”

“…These hypotheses treat the mammalian gomphosis as the most complex form of tooth attachment and posit that it has increased in complexity through evolutionary time in association with dental occlusion, culminating in the mammalian condition [10]. This view has been challenged more recently, because even when teeth are fused to the jaws, all amniote teeth possess homologous tooth attachment tissues to those in mammals [19,20,23]. These recent findings are re-framing our understanding of amniote dental evolution, but they still do not provide an evolutionary or developmental process to explain how mammals evolved a gomphosis from the ancestral synapsid condition of ankylosis.…”

Role of Cell Death in Cellular Processes During Odontogenesis

“…Programmed cell death rather helps to clear out the rest of the HERS cells which didn't migrate to adjacent periodontal ligament or differentiate into the cementoblasts (Kaneko et al, 1999). Even though HERS is present throughout the basal vertebrates and reptiles (Luan et al, 2006;LeBlanc et al, 2021) no sign of its disintegration has been described (with the exception of crocodilians); therefore the presence of apoptotic cells is not expected.…”

Epithelial Cell Rests of Malassez Provide a Favorable Microenvironment for Ameliorating the Impaired Osteogenic Potential of Human Periodontal Ligament Stem Cells

“…The periodontal ligament is a complex tissue that maintains various cell types such as PDLSCs, fibroblasts and epithelial cell rests of Malassez (ERM) (LeBlanc et al, 2020). Among them, ERM are the remaining epithelial cells of Hertwig's epithelial root sheath (HERS), which play important roles in maintaining the homeostasis of periodontal tissue (Yang et al, 2015) and preventing root resorption (Tsunematsu et al, 2016).…”