Micro-computed tomography imaging reveals the development of a unique tooth mineralization pattern in mackerel sharks (Chondrichthyes; Lamniformes) in deep time

Patrick L Jambura,René Kindlimann,David J Ward,Faviel López-Romero,Giuseppe Marramà,Jürgen Kriwet,Cathrin Pfaff,Julia Türtscher,Charlie J Underwood,Sebastian Stumpf

doi:10.1038/s41598-019-46081-3

Patrick L Jambura, René Kindlimann + Show 8 more

Open Access

https://doi.org/10.1038/s41598-019-46081-3

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Abstract

The cartilaginous fishes (Chondrichthyes) have a rich fossil record which consists mostly of isolated teeth and, therefore, phylogenetic relationships of extinct taxa are mainly resolved based on dental characters. One character, the tooth histology, has been examined since the 19th century, but its implications on the phylogeny of Chondrichthyes is still in debate. We used high resolution micro-CT images and tooth sections of 11 recent and seven extinct lamniform sharks to examine the tooth mineralization processes in this group. Our data showed similarities between lamniform sharks and other taxa (a dentinal core of osteodentine instead of a hollow pulp cavity), but also one feature that has not been known from any other elasmobranch fish: the absence of orthodentine. Our results suggest that this character resembles a synapomorphic condition for lamniform sharks, with the basking shark, Cetorhinus maximus, representing the only exception and reverted to the plesiomorphic tooth histotype. Additionally, †Palaeocarcharias stromeri, whose affiliation still is debated, shares the same tooth histology only known from lamniform sharks. This suggests that †Palaeocarcharias stromeri is member of the order Lamniformes, contradicting recent interpretations and thus, dating the origin of this group back at least into the Middle Jurassic.

Highlights

Lamniform sharks include some of the most iconic shark species, like the great white shark (Carcharodon carcharias) and the biggest macropredatory shark that has ever roamed the world’s oceans, †Otodus megalodon[1,2,3]
The oldest confirmed lamniform sharks are from the Valanginian (Early Cretaceous)[9], but the origin of this group remains ambiguous, because the systematic position of †Palaeocarcharias stromeri from the early Tithonian (Late Jurassic) remains unclear as being either a stem lamniform[10,11], an extinct sister group to lamniforms[12,13], or sister to a clade comprising Carcharhiniformes and Lamniformes[14]
We identified two different tooth mineralization patterns within lamniform sharks resulting in the osteodont and pseudoosteodont histotypes

Summary

Introduction

Lamniform sharks include some of the most iconic shark species, like the great white shark (Carcharodon carcharias) and the biggest macropredatory shark that has ever roamed the world’s oceans, †Otodus megalodon[1,2,3]. Www.nature.com/scientificreports tooth characters such as crown and root morphologies or root vascularization patterns mostly are the only features that can be used to infer the systematic position of extinct sharks[16,17]. Glickman[20,21] attempted to resolve the systematic positions of fossil chondrichthyans based solely on tooth histologies of the crown and introduced the concept of histotype inferring. He distinguished between two different tooth histologies - the orthodont and the osteodont tooth histotypes. The phylogeny of chondrichthyans has been drastically improved by adding more dental and morphological characters in recent years[5,27,28,29], the tooth histotype concept still is used to distinguish elasmobranch groups, as in rajiform and myliobatiform batomorphs[17,30] or in galeomorph sharks between lamniform and carcharhiniform sharks, with lamniforms displaying the osteodont tooth histotype and carcharhiniforms the orthodont histotype[26,31,32], with one exception: the carcharhiniform shark Hemipristis elongata that was assumed to have the osteodont tooth histology[16,17,25,33]

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