Mandibular biomechanics as a key factor to understand diet in mammals

The mammalian mandible plays a fundamental role in food processing, as it transmits the forces generated by masticatory muscles to the food through the teeth (MaynardSmith & Savage 1959). Generally speaking, the greater the forces required to fracture ingesta, and the more often such forces are needed, the stronger the mandible has to be to maintain its structural integrity (Hogue 2008). In that line, it has been suggested that among primates, those that include hard-food in their diets have stiffer mandibles when compared to soft-food eaters (Marcé-Nogué et al. 2017b). However, other attempts to establish relationships between mandibular morphology and dietary categories have not been particularly successful (Ross et al. 2012). If the latter is true and biomechanics cannot be used to establish relationships between morphology and function, it has been argued that it is probably because these biomechanical analyses are flawed or incomplete, or that nonmechanical factors such as phylogeny are more important determinants of morphology (Ross & Iriarte-Diaz 2014). Nevertheless, there is a general consensus that trying to understand the interaction between the mammalian feeding mechanism and the processed ingesta represents a unique opportunity for the study of ecomorphological adaptations in extant species, as well as having the potential to acquire valuable tools for the reconstruction of oral behaviors in extinct taxa. Hence the importance of this particular topic. The association between dietary preferences and biomechanical performance has traditionally been studied as the relationship between dental and mandibular morphology (Fig. 4.1). For example, carnivorous mammals have carnassials that act as blades allowing enlarged and often self-sharpening edges to pass by each other in a shearing manner. Herbivorous ungulates have developed reduced canine teeth and specialized molars to grind fibrous food by lateral movements. Among other examples, primates have teeth that exhibit an elaborated cusp pattern of the molars that crush the food (Kardong 2014). The way teeth work (e. g. blading, grinding, or crushing) is adapted to the diet as well as the morphology of the mandibles, thus enabling the generation of different models of distribution and position of the muscular forces and bite positions based on different geometries (Vizcaíno et al. 2016). The influence of muscular forces on the design of the shape of the mandible (e. g., Sella-Tunis et al. 2018 in humans), as well as the influence of the position of the condyle allowing different mandible movements (Maynard-Smith & Savage 1959) are evidence that reinforces the idea that food is processed differently depending on mandibular morphology. For these reasons, feeding biomechanics represents the set of analyses performed to “[. ] relate variation in feeding system morphology (size and shape of muscles, bones, teeth, tongues or joints) to variation in how animals feed (feeding behavior) and what they feed on (diet). ” (Ross & Iriarte-Diaz 2014: 105). This relationship between muscular and bite forces, mandibular size and shape, and the consumed ingesta have previously been studied in the mandibles of different mammalian clades such as terrestrial Cetartiodactyla (Christiansen & Wroe 2007, Hogue & Ravosa 2001, Spencer 1995, Varela & Fariña 2015), Chiroptera (Freeman 1979, 1981, 1984, 1988, 2000), Primates (Bouvier 1986a,b, Taylor 2006) and Carnivora (Biknevicius & Ruff 1992, Radinsky 1981a,b). These works used classical biomechanics based on the laws of static mechanics and beam theory, hence not requiring the application of computer simulation techniques to model complex biological geometries, thus avoiding a high computational cost. The eruption of computational methods opened a whole array of new possibilities to investigate feeding biomechanics. Specifically, computational biomechanics represents the application of engineering computational tools, such as the finite element analysis (FEA) (Zienkiewicz & Taylor 1981) to study the mechanics of biological systems. Computational models and simulations are particularly useful to predict the relationship between parameters that are otherwise challenging to test using experimental approaches and are also quite helpful when designing more relevant experiments, hence reducing the time and costs of such tests. The underlying premise of the method is that a complex geometry can be subdivided into a mesh consisting of a number of finite elements in which the respective mechanical equations are approximately solved. Although FEA (see Rayfield 2007 for a review) or multibody dynamic analysis (see Curtis 2011 for a review of MDA) have been common approaches in engineering and biomedicine for more than thirty years, they have also been applied to biological research in order to address questions related to biomechanics and the evolution of living and extinct vertebrates (using both 2D or high-resolution 3D models). Vertebrate paleontologists have also applied complementary non-invasive techniques, such as computed tomography (CT), which is a useful tool to generate accurate 3D images of living structures in a reverse engineering process, thus facilitating the application of computational biomechanics. The reliability and bio-fidelity of the biomechanical models has increasingly improved by capturing the real geometries of the specimens under analysis. Previous approaches Mandibular biomechanics as a key factor to understand diet in mammals