Tooth mineralization and histology patterns in extinct and extant snaggletooth sharks, Hemipristis (Carcharhiniformes, Hemigaleidae)-Evolutionary significance or ecological adaptation?

Patrick L Jambura,Charlie J Underwood,Cathrin Pfaff,Jürgen Kriwet,David J Ward,Alistair Robert Evans

doi:10.1371/journal.pone.0200951

Patrick L Jambura, Charlie J Underwood + Show 4 more

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https://doi.org/10.1371/journal.pone.0200951

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Abstract

Shark jaws exhibit teeth that are arranged into distinct series and files and display great diversities in shapes and structures, which not only is related to their function (grasping, cutting, crushing) during feeding, but also bear a strong phylogenetic signal. So far, most research on the relationship between shark teeth and feeding ecology and systematics focused on the external tooth morphology only. Although the tooth histology of sharks has been examined since the early 19th century, its functional and systematic implications are still ambiguous. Shark teeth normally consist of either a porous, cellular dentine, osteodentine (in lamniform sharks and some batoids) or a dense layer of orthodentine (known from different sharks). Sharks of the order Carcharhiniformes, comprising ca. 60% of all extant shark species, are known to have orthodont teeth, with a single exception—the snaggletooth shark, Hemipristis elongata. High resolution micro-CT images of jaws and teeth from selected carcharhiniform sharks (including extant and fossil snaggletooth sharks) and tooth sections of teeth of Hemipristis, other carcharhiniform and lamniform sharks, have revealed that (1) Hemipristis is indeed the only carcharhiniform shark filling its pulp cavity with osteodentine in addition to orthodentine, (2) the tooth histology of Hemipristis elongata differs from the osteodont histotype, which evolved in lamniform sharks and conversely represents a modified orthodonty, and (3) this modified orthodonty was already present in extinct Hemipristis species but the mineralization sequence has changed over time. Our results clearly show the presence of a third tooth histotype—the pseudoosteodont histotype, which is present in Hemipristis. The unique tooth histology of lamniform sharks might provide a phylogenetic signal for this group, but more research is necessary to understand the phylogenetic importance of tooth histology in sharks in general.

Highlights

Sharks possess a constantly forming series of teeth in which functional teeth are replaced in succession [1,2,3]
Five jaws analysed here are from hemigaleid sharks, six jaws are from carcharhinid sharks (Carcharhinus melanopterus, C. obscurus, C. signatus, Galeocerdo cuvier, Prionace glauca, Rhizoprionodon acutus) and one jaw is from a sphyrnid shark (Sphyrna zygaena) (Table 1)
In this study we unambiguously demonstrate that the pseudoosteodont tooth histology found in Hemipristis elongata differs from the osteodont type found in lamniform sharks and, indicates that the development of similar tooth histologies represent convergent evolution

Summary

Introduction

Sharks possess a constantly forming series of teeth in which functional teeth are replaced in succession (polyphydont dentition) [1,2,3]. There are two main different patterns how teeth can be arranged within the jaw They either are added alternatingly within two adjacent tooth series (double vertical row; alternate dentition) or in single tooth files (single vertical row; independent dentition) [4,5,6] with teeth being shed individually (e.g. in carcharhiniform sharks) [4,6] or in groups up to entire tooth rows (e.g. squaliform sharks) [4,7]. The number of teeth in an erect position within each tooth file varies between species These erect teeth are the ones in use and are considered functional teeth, teeth in a semi-erect or inverted position form the developing replacement teeth [4]

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