Abstract

The progressive character of tooth formation records aspects of mammalian life history, diet, seasonal behavior and climate. Tooth mineralization occurs in two stages: secretion and maturation, which overlap to some degree. Despite decades of study, the spatial and temporal pattern of elemental incorporation during enamel mineralization remains poorly characterized. Here we use synchrotron X-ray microtomography and Markov Chain Monte Carlo sampling to estimate mineralization patterns from an ontogenetic series of sheep molars (n = 45 M1s, 18 M2s). We adopt a Bayesian approach that posits a general pattern of maturation estimated from individual- and population-level mineral density variation over time. This approach converts static images of mineral density into a dynamic model of mineralization, and demonstrates that enamel secretion and maturation waves advance at nonlinear rates with distinct geometries. While enamel secretion is ordered, maturation geometry varies within a population and appears to be driven by diffusive processes. Our model yields concrete expectations for the integration of physiological and environmental signals, which is of particular significance for paleoseasonality research. This study also provides an avenue for characterizing mineralization patterns in other taxa. Our synchrotron imaging data and model are available for application to multiple disciplines, including health, material science, and paleontological research.

Highlights

  • Teeth form incrementally, creating microscopic features that have been a subject of study since they were first observed by van Leeuwenhoek in the 17th century [1,2,3,4]

  • Our virtual sections show maturation geometry is variable across individuals and times during formation (Fig 3)

  • By standardizing M1 shapes and assembling mineralization trajectories (S1 File) into a dynamic mineralization model (Fig 6), we find that secretion and maturation proceed in two waves that are distinct in geometry and timing (Fig 7; S2 File)

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Summary

Introduction

Teeth form incrementally, creating microscopic features that have been a subject of study since they were first observed by van Leeuwenhoek in the 17th century [1,2,3,4]. Enamel mineralization is traditionally conceptualized in two stages: secretion and maturation (S1 Text) [12,13,14]. While secretion is well characterized, maturation–when most mineral is incorporated–has been difficult to study and remains poorly understood [15,16,17,18,19], limiting applications in a variety of disciplines [20,21,22,23,24,25,26,27,28,29,30]. This study uses synchrotron density characterization to resolve uncertainty in the nature of enamel maturation, describing its timing and geometry, relationship to secretion, and variation within a population of animals

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