Evolutionary trajectories of tooth histology patterns in modern sharks (Chondrichthyes, Elasmobranchii).

Patrick L Jambura,Brian Metscher,Sebastian Stumpf,Julia Türtscher,Gerhard W Weber,Cathrin Pfaff,René Kindlimann,Jürgen Kriwet

doi:10.1111/joa.13145

Abstract

During their evolutionary history, modern sharks developed different tooth mineralization patterns that resulted in very distinct histological patterns of the tooth crown (histotypes). To date, three different tooth histotypes have been distinguished: (i) orthodont teeth, which have a central hollow pulp cavity in the crown, encapsulated by a prominent layer of dentine (orthodentine); (ii) pseudoosteodont teeth, which have their pulp cavities secondarily replaced by a dentinal core of porous dentine (osteodentine), encased by orthodentine; and (iii) osteodont teeth, which lack orthodentine and the whole tooth crown of which consists of osteodentine. The aim of the present study was to trace evolutionary trends of tooth mineralization patterns in modern sharks and to find evidence for the presence of phylogenetic or functional signals. High resolution micro‐computed tomography images were generated for the teeth of members of all nine extant shark orders and the putative stem group †Synechodontiformes, represented here by three taxa, to examine the tooth histology non‐destructively. Pseudoosteodonty is the predominant state among modern sharks and represents unambiguously the plesiomorphic condition. Orthodonty evolved several times independently in modern sharks, while the osteodont tooth histotype is only developed in lamniform sharks. The two shark orders Heterodontiformes and Pristiophoriformes showed highly modified tooth histologies, with Pristiophorus exhibiting a histology only known from batomorphs (i.e. rays and skates), and Heterodontus showing a histological difference between anterior and posterior teeth, indicating a link between its tooth morphology, histology and durophagous lifestyle. The tooth histotype concept has proven to be a useful tool to reflect links between histology, function and its taxonomic value for distinct taxa; however, a high degree of variation, especially in the pseudoosteodont tooth histotype, demonstrates that the current histotype concept is too simplistic to fully resolve these relationships. The vascularization pattern of the dentine might offer new future research pathways for better understanding functional and phylogenetic signals in the tooth histology of modern sharks.

Highlights

More recent studies defined three histotypes, depending on the presence or absence of orthodentine and osteodentine in the crown: (i) orthodont teeth, which have a central hollow pulp cavity, encapsulated by a substantial layer of orthodentine; (ii) pseudoosteodont teeth, in which osteodentine intrudes from the root into the hollow pulp cavity, which in fully mineralized teeth is replaced by an osteodont core that is surrounded by orthodentine; and (iii) osteodont teeth, in which no orthodentine is developed, but the complete dentinal core of the crown consists of osteodentine and replaces the hollow pulp cavity (Jambura et al 2018; Jambura et al 2019)
Our findings demonstrate that the pseudoosteodont tooth histotype is the most common tooth histology in modern sharks
In this study we examined the tooth histology patterns in modern sharks of all nine extant orders plus members of the stem group †Synechodontiformes and investigated the evolutionary significance of the different tooth histologies

Summary

Introduction

Modern sharks form a monophyletic group with rays and skates (Neoselachii sensu Compagno, 1977; Elasmobranchii sensu Maisey, 2012), with a fossil record extending back into the Early Permian (295 mya; Ivanov, 2005) and haveShark teeth can be subdivided into two external portions: the root, which is attached to a set of connective tissues enveloping the oral jaw cartilage surfaces (Peyer, 1968; Rasch et al 2016; Smith et al 2018) and the crown, which is used for prey capture during the feeding process (Compagno, 1988). Orthodentine exhibits parallel, branching tubules that were originally described to surround a hollow pulp cavity (Radinsky, 1961; Smith & Sansom, 2000), but which can surround a dentinal core of osteodentine in shark teeth (Jambura et al 2018)). Two histological patterns were distinguished in shark teeth, the orthodont histotype (presence of a hollow pulp cavity) and the osteodont histotype [the pulp cavity is replaced by osteodentine that extends from the root (Tomes, 1876; Glickman, 1964; Compagno, 1988; Moyer et al 2015; Schnetz et al 2016; Martınez-Perez et al 2018)]. More recent studies defined three histotypes, depending on the presence or absence of orthodentine and osteodentine in the crown: (i) orthodont teeth, which have a central hollow pulp cavity, encapsulated by a substantial layer of orthodentine; (ii) pseudoosteodont teeth, in which osteodentine intrudes from the root into the hollow pulp cavity, which in fully mineralized teeth is replaced by an osteodont core that is surrounded by orthodentine; and (iii) osteodont teeth, in which no orthodentine is developed, but the complete dentinal core of the crown consists of osteodentine and replaces the hollow pulp cavity (Jambura et al 2018; Jambura et al 2019)

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