Adaptations in the structure, composition and properties of primate tooth enamel
Creators: name: Foster, Frederick Robert
Publisher: name: No Publisher Supplied
Year: 2022

description: All animals need energy and nutrients to survive, to compete for resources, and to facilitate reproduction. Energy and nutrients are bound inside the foods consumed by animals and are freed during digestion. Chewing is one of the earliest steps in digestion, when food particles are in their most mechanically challenging state. This makes tooth enamel one of the most important tissues in the body, because it works early in digestion to free energy and nutrients by crushing, grinding, and tearing mechanically challenging food particles. Teeth that work well and last long will promote foraging and digestive efficiency, and an extended lifespan that ultimately increases fitness. Teeth that function poorly, or fail outright, will decrease foraging and digestive efficiency, and increase the risk of dental disease that can truncate lifespan and lower overall fitness.These factors have made enamel the center of many studies that seek to identify signals of selection and dietary adaptation in human and non-human primate evolution. The conclusions of these studies are based on a tenuous understanding of how enamel functions during chewing, why it can cope with high bite forces and countless chew cycles, and the circumstances that ultimately result in tooth failure within and across species. This dissertation looks inside the enamel layer, at its mechanical properties, chemical composition, and microstructure to determine its role in dietary behavior and identify signals of adaptation. The results have implications for previous work that has treated enamel as a simple and internally homogenous material. Not all enamel is created equal; the underexplored adaptations that exist within the enamel layer are equally as important as the well-hewn fields of research that describe the adaptations without.This dissertation used nanoindentation to measure mechanical properties throughout the enamel crown in a sample of twenty-two specimens across ten species of non-human primates. Nanoindentation is a common method used in the material sciences to measure the stiffness and hardness of a material at very small spatial scales, which is helpful for measuring variation within primate enamel that is rarely thicker than 1 mm. High stiffness and hardness are key features of enamel, inherited from its principal component, mineral hydroxyapatite, that help teeth transmit bite forces during chewing while resisting failure. These properties were found to vary throughout the enamel crown of primates, with implications for dental function.The highest average values for enamel stiffness were seen in the animals that can generate the highest bite forces, chimpanzees, and the animals that consume the most challenging diets, tufted capuchins. This was interpreted as an adaptation to more efficiently transmit bite forces into food particles while chewing. However, high stiffness means a greater risk of for fracture and significant decreases in stiffness were found in areas of the enamel crown that are associated with fracture propagation while chewing. Across all specimens, significantly lower stiffness was observed in the base of the crown and interpreted as an adaptation to reduce the risk of fractures in a region that is vulnerable to fracture after many chew cycles. Significant decreases in stiffness were also observed at the junction between the brittle enamel layer and the more pliable dentine. Here, low stiffness was viewed as an adaptation to protect the sensitive juncture between these two tissues from fractures when dentine deforms due to high bite forces. High hardness is associated with wear resistance, and it was highest across all specimens in the cusps where occlusal contact between teeth and food particles is made. Within the cusps hardness peaked near the enamel surface, which was interpreted as an adaptation to slow the wear rate and extend the use-life of the tooth.The mechanical properties of enamel are emergent properties of its underlying chemical composition and microstructure. Electron microprobe analysis was used to measure the primary mineral components and trace elements of enamel, and to calculate an estimate of the protein and water fraction. These measurements were tightly paired with the nanoindentation results at small spatial scales that allowed for a more confident correlation analyses than previous studies have offered. The results show that the protein and water fraction is significantly related to the mechanical properties of enamel. Enamel stiffness was lowest in regions where the protein and water fraction was highest. Trace elements were implicated in the processes that establish the increased protein and water content, where Mg and Na cations appear to substitute for Ca cations in the hydroxyapatite crystallite lattice. These substitutions can inhibit hydroxyapatite crystallite growth in developing enamel, leaving a higher protein and water content and lower stiffness. Though significant, the correlation strength between mechanical properties and chemistry suggests that other factors are important for determining stiffness and hardness in enamel.Microstructure was investigated using a novel method that combined nanoindentation with acid etching and microscopy to image the underlying tissue. This allowed for direct correlation between the results of nanoindentation and features of the microstructure that have been previously implicated as drivers of the variation in mechanical properties. The results showed that nanoindentation can distinguish between features of enamel prisms and the interprismatic matrix, but not between prisms that intersect the testing surface at different angles. This finding challenges the results of studies that make qualitative comparisons between nanoindentation results and images of enamel microstructure. Instead, the density of prisms, and the protein and water fraction were found to be stronger predictors of stiffness and hardness, respectively. This lends support to an interpretation of enamel as a composite structure, where stiff prisms bear the loads of bite forces while reduced stiffness in interprismatic matrix enamel distributes transverse loads between them. The results also reinforce the importance of the protein and water content of enamel to its mechanical function. Future research is directed towards a functional understanding of proteins and the extracellular makeup of developing enamel.