Mechanical compensation in the evolution of the early hominin feeding apparatus.

Australopiths, a group of hominins from the Plio-Pleistocene of Africa, are characterized by derived traits in their crania hypothesized to strengthen the facial skeleton against feeding loads and increase the efficiency of bite force production. The crania of robust australopiths are further thought to be stronger and more efficient than those of gracile australopiths. Results of prior mechanical analyses have been broadly consistent with this hypothesis, but here we show that the predictions of the hypothesis with respect to mechanical strength are not met: some gracile australopith crania are as strong as that of a robust australopith, and the strength of gracile australopith crania overlaps substantially with that of chimpanzee crania. We hypothesize that the evolution of cranial traits that increased the efficiency of bite force production in australopiths may have simultaneously weakened the face, leading to the compensatory evolution of additional traits that reinforced the facial skeleton. The evolution of facial form in early hominins can therefore be thought of as an interplay between the need to increase the efficiency of bite force production and the need to maintain the structural integrity of the face.

Fracture mechanics, enamel thickness and the evolution of molar form in hominins.

As the tissue most directly responsible for breaking down food in the oral cavity, the form and function of enamel is obviously of evolutionary significance in humans, non-human primates and other vertebrates. Accordingly, a standard metric, relative enamel thickness (RET), has been used for many decades to provide insights into vertebrate and human palaeobiology. Relatively thick enamel has evolved many times in vertebrates including hominoids (the group to which living humans and fossil hominins belong), and this pattern is thought to provide information about taxonomy, phylogeny, functional anatomy and diet. In particular, relatively thick enamel is thought to make tooth crowns strong so that they resist fractures associated with eating mechanically resistant foods. Here, we use current models of tooth biomechanics to show that RET is at best only moderately informative of function and diet in living hominoids and fossil hominins, and at worst provides misleading information. We propose a new metric, absolute crown strength, to assess the resistance of teeth to fracture, and identify what may be a novel characteristic of tooth strength in fossil hominins.

Taking a big bite: Working together to better understand the evolution of feeding in primates.

The study of adaptation requires the integration of an array of different types of data. A single individual can find such integration daunting, if not impossible. In an effort to clarify the role of diet in the evolution of the primate craniofacial and dental apparatus, we assembled a team of researchers that have various types and degrees of expertise. This interaction has provided a range of insights for all contributors, and this has helped to refine questions, clarify the possibilities and limitations that laboratory and field settings offer, and further explore the ways in which laboratory and field data can be suitably integrated. A complete and accurate picture of dietary adaptation cannot be gained in isolation. Collaboration provides the bridge to a more holistic view of primate biology and evolution.

Viewpoints: diet and dietary adaptations in early hominins: the hard food perspective.

Recent biomechanical analyses examining the feeding adaptations of early hominins have yielded results consistent with the hypothesis that hard foods exerted a selection pressure that influenced the evolution of australopith morphology. However, this hypothesis appears inconsistent with recent reconstructions of early hominin diet based on dental microwear and stable isotopes. Thus, it is likely that either the diets of some australopiths included a high proportion of foods these taxa were poorly adapted to consume (i.e., foods that they would not have processed efficiently), or that aspects of what we thought we knew about the functional morphology of teeth must be wrong. Evaluation of these possibilities requires a recognition that analyses based on microwear, isotopes, finite element modeling, and enamel chips and cracks each test different types of hypotheses and allow different types of inferences. Microwear and isotopic analyses are best suited to reconstructing broad dietary patterns, but are limited in their ability to falsify specific hypotheses about morphological adaptation. Conversely, finite element analysis is a tool for evaluating the mechanical basis of form-function relationships, but says little about the frequency with which specific behaviors were performed or the particular types of food that were consumed. Enamel chip and crack analyses are means of both reconstructing diet and examining biomechanics. We suggest that current evidence is consistent with the hypothesis that certain derived australopith traits are adaptations for consuming hard foods, but that australopiths had generalized diets that could include high proportions of foods that were both compliant and tough.

The biomechanics of tooth strength: testing the utility of simple models for predicting fracture in geometrically complex teeth.

Teeth must fracture foods while avoiding being fractured themselves. This study evaluated dome biomechanical models used to describe tooth strength. Finite-element analysis (FEA) tested whether the predictions of the dome models applied to the complex geometry of an actual tooth. A finite-element model was built from microCT scans of a human M3. The FEA included three loading regimes simulating contact between (i) a hard object and a single cusp tip, (ii) a hard object and all major cusp tips and (iii) a soft object and the entire occlusal basin. Our results corroborate the dome models with respect to the distribution and orientation of tensile stresses, but document heterogeneity of stress orientation across the lateral enamel. This implies that high stresses might not cause fractures to fully propagate between cusp tip and cervix under certain loading conditions. The crown is most at risk of failing during hard object biting on a single cusp. Geometrically simple biomechanical models are valuable tools for understanding tooth function but do not fully capture aspects of biomechanical performance in actual teeth whose complex geometries may reflect adaptations for strength.

Microwear, mechanics and the feeding adaptations of Australopithecus africanus.

Recent studies of dental microwear and craniofacial mechanics have yielded contradictory interpretations regarding the feeding ecology and adaptations of Australopithecus africanus. As part of this debate, the methods used in the mechanical studies have been criticized. In particular, it has been claimed that finite element analysis has been poorly applied to this research question. This paper responds to some of these mechanical criticisms, highlights limitations of dental microwear analysis, and identifies avenues of future research.

Probabilistic finite element analysis of a craniofacial finite element model.

We employed a probabilistic finite element analysis (FEA) method to determine how variability in material property values affects stress and strain values in a finite model of a Macaca fascicularis cranium. The material behavior of cortical bone varied in three ways: isotropic homogeneous, isotropic non-homogeneous, and orthotropic non-homogeneous. The material behavior of the trabecular bone and teeth was always treated as isotropic and homogeneous. All material property values for the cranium were randomized with a Gaussian distribution with either coefficients of variation (CVs) of 0.2 or with CVs calculated from empirical data. Latin hypercube sampling was used to determine the values of the material properties used in the finite element models. In total, four hundred and twenty six separate deterministic FE simulations were executed. We tested four hypotheses in this study: (1) uncertainty in material property values will have an insignificant effect on high stresses and a significant effect on high strains for homogeneous isotropic models; (2) the effect of variability in material property values on the stress state will increase as non-homogeneity and anisotropy increase; (3) variation in the in vivo shear strain values reported by Strait et al. (2005) and Ross et al. (2011) is not only due to variations in muscle forces and cranial morphology, but also due to variation in material property values; (4) the assumption of a uniform coefficient of variation for the material property values will result in the same trend in how moderate-to-high stresses and moderate-to-high strains vary with respect to the degree of non-homogeneity and anisotropy as the trend found when the coefficients of variation for material property values are calculated from empirical data. Our results supported the first three hypotheses and falsified the fourth. When material properties were varied with a constant CV, as non-homogeneity and anisotropy increased the level of variability in the moderate-to-high strains decreased while the level of variability in the moderate-to-high stresses increased. However, this is not the pattern observed when CVs calculated from empirical data were applied to the material properties where the lowest level of variability in both stresses and strains occurred when the cranium was modeled with a low level of non-homogeneity and anisotropy. Therefore, when constant material property variability is assumed, inaccurate trends in the level of variability present in modest-to-high magnitude stresses and strains are produced. When the cranium is modeled with the highest level of accuracy (high non-homogeneity and anisotropy) and when randomness in the material properties is calculated from empirical data, there is a large level of variability in the significant strains (CV=0.369) and a low level of variability in the modest-to-high magnitude stresses (CV=0.150). This result may have important implications with regard to the mechanical signals driving bone remodeling and adaptation through natural selection.

The feeding biomechanics and dietary ecology of Australopithecus africanus.

The African Plio-Pleistocene hominins known as australopiths evolved a distinctive craniofacial morphology that traditionally has been viewed as a dietary adaptation for feeding on either small, hard objects or on large volumes of food. A historically influential interpretation of this morphology hypothesizes that loads applied to the premolars during feeding had a profound influence on the evolution of australopith craniofacial form. Here, we test this hypothesis using finite element analysis in conjunction with comparative, imaging, and experimental methods. We find that the facial skeleton of the Australopithecus type species, A. africanus, is well suited to withstand premolar loads. However, we suggest that the mastication of either small objects or large volumes of food is unlikely to fully explain the evolution of facial form in this species. Rather, key aspects of australopith craniofacial morphology are more likely to be related to the ingestion and initial preparation of large, mechanically protected food objects like large nuts and seeds. These foods may have broadened the diet of these hominins, possibly by being critical resources that australopiths relied on during periods when their preferred dietary items were in short supply. Our analysis reconciles apparent discrepancies between dietary reconstructions based on biomechanics, tooth morphology, and dental microwear.

The cranial biomechanics and feeding performance of Homo floresiensis.

Homo floresiensis is a small-bodied hominin from Flores, Indonesia, that exhibits plesiomorphic dentognathic features, including large premolars and a robust mandible, aspects of which have been considered australopith-like. However, relative to australopith species, H. floresiensis exhibits reduced molar size and a cranium with diminutive midfacial dimensions similar to those of later Homo, suggesting a reduction in the frequency of forceful biting behaviours. Our study uses finite-element analysis to examine the feeding biomechanics of the H. floresiensis cranium. We simulate premolar (P3) and molar (M2) biting in a finite-element model (FEM) of the H. floresiensis holotype cranium (LB1) and compare the mechanical results with FEMs of chimpanzees, modern humans and a sample of australopiths (MH1, Sts 5, OH5). With few exceptions, strain magnitudes in LB1 resemble elevated levels observed in modern Homo. Our analysis of LB1 suggests that H. floresiensis could produce bite forces with high mechanical efficiency, but was subject to tensile jaw joint reaction forces during molar biting, which perhaps constrained maximum postcanine bite force production. The inferred feeding biomechanics of H. floresiensis closely resemble modern humans, suggesting that this pattern may have been present in the last common ancestor of Homo sapiens and H. floresiensis.

An infant burial from Arma Veirana in northwestern Italy provides insights into funerary practices and female personhood in early Mesolithic Europe.

The evolution and development of human mortuary behaviors is of enormous cultural significance. Here we report a richly-decorated young infant burial (AVH-1) from Arma Veirana (Liguria, northwestern Italy) that is directly dated to 10,211-9910 cal BP (95.4% probability), placing it within the early Holocene and therefore attributable to the early Mesolithic, a cultural period from which well-documented burials are exceedingly rare. Virtual dental histology, proteomics, and aDNA indicate that the infant was a 40-50 days old female. Associated artifacts indicate significant material and emotional investment in the child's interment. The detailed biological profile of AVH-1 establishes the child as the earliest European near-neonate documented to be female. The Arma Veirana burial thus provides insight into sex/gender-based social status, funerary treatment, and the attribution of personhood to the youngest individuals among prehistoric hunter-gatherer groups and adds substantially to the scant data on mortuary practices from an important period in prehistory shortly following the end of the last Ice Age.

Ingestive behaviors in bearded capuchins (Sapajus libidinosus).

The biomechanical and adaptive significance of variation in craniodental and mandibular morphology in fossil hominins is not always clear, at least in part because of a poor understanding of how different feeding behaviors impact feeding system design (form-function relationships). While laboratory studies suggest that ingestive behaviors produce variable loading, stress, and strain regimes in the cranium and mandible, understanding the relative importance of these behaviors for feeding system design requires data on their use in wild populations. Here we assess the frequencies and durations of manual, ingestive, and masticatory behaviors from more than 1400 observations of feeding behaviors video-recorded in a wild population of bearded capuchins (Sapajus libidinosus) at Fazenda Boa Vista in Piauí, Brazil. Our results suggest that ingestive behaviors in wild Sapajus libidinosus were used for a range of food material properties and typically performed using the anterior dentition. Coupled with previous laboratory work indicating that ingestive behaviors are associated with higher mandibular strain magnitudes than mastication, these results suggest that ingestive behaviors may play an important role in craniodental and mandibular design in capuchins and may be reflected in robust adaptations in fossil hominins.

Hard plant tissues do not contribute meaningfully to dental microwear: evolutionary implications.

Reconstructing diet is critical to understanding hominin adaptations. Isotopic and functional morphological analyses of early hominins are compatible with consumption of hard foods, such as mechanically-protected seeds, but dental microwear analyses are not. The protective shells surrounding seeds are thought to induce complex enamel surface textures characterized by heavy pitting, but these are absent on the teeth of most early hominins. Here we report nanowear experiments showing that the hardest woody shells - the hardest tissues made by dicotyledonous plants - cause very minor damage to enamel but are themselves heavily abraded (worn) in the process. Thus, hard plant tissues do not regularly create pits on enamel surfaces despite high forces clearly being associated with their oral processing. We conclude that hard plant tissues barely influence microwear textures and the exploitation of seeds from graminoid plants such as grasses and sedges could have formed a critical element in the dietary ecology of hominins.

Allometry, sexual dimorphism, and phylogeny: a cladistic analysis of extant African papionins using craniodental data.

This study conducts a phylogenetic analysis of extant African papionin craniodental morphology, including both quantitative and qualitative characters. We use two different methods to control for allometry: the previously described narrow allometric coding method, and the general allometric coding method, introduced herein. The results of this study strongly suggest that African papionin phylogeny based on molecular systematics, and that based on morphology, are congruent and support a Cercocebus/Mandrillus clade as well as a Papio/Lophocebus/Theropithecus clade. In contrast to previous claims regarding papionin and, more broadly, primate craniodental data, this study finds that such data are a source of valuable phylogenetic information and removes the basis for considering hard tissue anatomy "unreliable" in phylogeny reconstruction. Among highly sexually dimorphic primates such as papionins, male morphologies appear to be particularly good sources of phylogenetic information. In addition, we argue that the male and female morphotypes should be analyzed separately and then added together in a concatenated matrix in future studies of sexually dimorphic taxa. Character transformation analyses identify a series of synapomorphies uniting the various papionin clades that, given a sufficient sample size, should potentially be useful in future morphological analyses, especially those involving fossil taxa.

Evidence that metallic proxies are unsuitable for assessing the mechanics of microwear formation and a new theory of the meaning of microwear.

Mammalian tooth wear research reveals contrasting patterns seemingly linked to diet: irregularly pitted enamel surfaces, possibly from consuming hard seeds, versus roughly aligned linearly grooved surfaces, associated with eating tough leaves. These patterns are important for assigning diet to fossils, including hominins. However, experiments establishing conditions necessary for such damage challenge this paradigm. Lucas et al. (Lucas et al. 2013 J. R. Soc. Interface10, 20120923. (doi:10.1098/rsif.2012.0923)) slid natural objects against enamel, concluding anything less hard than enamel would rub, not abrade, its surface (producing no immediate wear). This category includes all organic plant matter. Particles harder than enamel, with sufficiently angular surfaces, could abrade it immediately, prerequisites that silica/silicate particles alone possess. Xia et al. (Xia, Zheng, Huang, Tian, Chen, Zhou, Ungar, Qian. 2015 Proc. Natl Acad. Sci. USA112, 10 669-10 672. (doi:10.1073/pnas.1509491112)) countered with experiments using brass and aluminium balls. Their bulk hardness was lower than enamel, but the latter was abraded. We examined the ball exteriors to address this discrepancy. The aluminium was surfaced by a thin rough oxide layer harder than enamel. Brass surfaces were smoother, but work hardening during manufacture gave them comparable or higher hardness than enamel. We conclude that Xia et al.'s results are actually predicted by the mechanical model of Lucas et al. To explain wear patterns, we present a new model of textural formation, based on particle properties and presence/absence of silica(tes).

The Biomechanics of Bony Facial "Buttresses" in South African Australopiths: An Experimental Study Using Finite Element Analysis.

Australopiths exhibit a number of derived facial features that are thought to strengthen the face against high and/or repetitive loads associated with a diet that included mechanically challenging foods. Here, we use finite element analysis (FEA) to test hypotheses related to the purported strengthening role of the zygomatic root and "anterior pillar" in australopiths. We modified our previously constructed models of Sts 5 (Australopithecus africanus) and MH1 (A. sediba) to differ in the morphology of the zygomatic root, including changes to both the shape and positioning of the zygomatic root complex, in addition to creating variants of Sts 5 lacking anterior pillars. We found that both an expanded zygomatic root and the presence of "anterior pillars" reinforce the face against feeding loads. We also found that strain orientations are most compatible with the hypothesis that the pillar evolved to resist loads associated with premolar loading, and that this morphology has an ancillary effect of strengthening the face during all loading regimes. These results provide support for the functional hypotheses. However, we found that an anteriorly positioned zygomatic root increases strain magnitudes even in models with an inflated/reinforced root complex. These results suggest that an anteriorly placed zygomatic root complex evolved to enhance the efficiency of bite force production while facial reinforcement features, such as the anterior pillar and the expanded zygomatic root, may have been selected for in part to compensate for the weakening effect of this facial configuration. Anat Rec, 300:171-195, 2017. © 2016 Wiley Periodicals, Inc.

Review of In Vivo Bone Strain Studies and Finite Element Models of the Zygomatic Complex in Humans and Nonhuman Primates: Implications for Clinical Research and Practice.

The craniofacial skeleton is often described in the clinical literature as being comprised of vertical bony pillars, which transmit forces from the toothrow to the neurocranium as axial compressive stresses, reinforced transversely by buttresses. Here, we review the literature on bony microarchitecture, in vivo bone strain, and finite-element modeling of the facial skeleton of humans and nonhuman primates to address questions regarding the structural and functional existence of facial pillars and buttresses. Available bone material properties data do not support the existence of pillars and buttresses in humans or Sapajus apella. Deformation regimes in the zygomatic complex emphasize bending and shear, therefore conceptualizing the zygomatic complex of humans or nonhuman primates as a pillar obscures its patterns of stress, strain, and deformation. Human fossil relatives and chimpanzees exhibit strain regimes corroborating the existence of a canine-frontal pillar, but the notion of a zygomatic pillar has no support. The emerging consensus on patterns of strain and deformation in finite element models (FEMs) of the human facial skeleton corroborates hypotheses in the clinical literature regarding zygomatic complex function, and provide new insights into patterns of failure of titanium and resorbable plates in experimental studies. It is suggested that the "pillar and buttress" model of human craniofacial skeleton function be replaced with FEMs that more accurately and precisely represent in vivo function, and which can serve as the basis for future research into implants used in restoration of occlusal function and fracture repair. Anat Rec, 299:1753-1778, 2016. © 2016 Wiley Periodicals, Inc.

Human feeding biomechanics: performance, variation, and functional constraints.

The evolution of the modern human (Homo sapiens) cranium is characterized by a reduction in the size of the feeding system, including reductions in the size of the facial skeleton, postcanine teeth, and the muscles involved in biting and chewing. The conventional view hypothesizes that gracilization of the human feeding system is related to a shift toward eating foods that were less mechanically challenging to consume and/or foods that were processed using tools before being ingested. This hypothesis predicts that human feeding systems should not be well-configured to produce forceful bites and that the cranium should be structurally weak. An alternate hypothesis, based on the observation that humans have mechanically efficient jaw adductors, states that the modern human face is adapted to generate and withstand high biting forces. We used finite element analysis (FEA) to test two opposing mechanical hypotheses: that compared to our closest living relative, chimpanzees (Pan troglodytes), the modern human craniofacial skeleton is (1) less well configured, or (2) better configured to generate and withstand high magnitude bite forces. We considered intraspecific variation in our examination of human feeding biomechanics by examining a sample of geographically diverse crania that differed notably in shape. We found that our biomechanical models of human crania had broadly similar mechanical behavior despite their shape variation and were, on average, less structurally stiff than the crania of chimpanzees during unilateral biting when loaded with physiologically-scaled muscle loads. Our results also show that modern humans are efficient producers of bite force, consistent with previous analyses. However, highly tensile reaction forces were generated at the working (biting) side jaw joint during unilateral molar bites in which the chewing muscles were recruited with bilateral symmetry. In life, such a configuration would have increased the risk of joint dislocation and constrained the maximum recruitment levels of the masticatory muscles on the balancing (non-biting) side of the head. Our results do not necessarily conflict with the hypothesis that anterior tooth (incisors, canines, premolars) biting could have been selectively important in humans, although the reduced size of the premolars in humans has been shown to increase the risk of tooth crown fracture. We interpret our results to suggest that human craniofacial evolution was probably not driven by selection for high magnitude unilateral biting, and that increased masticatory muscle efficiency in humans is likely to be a secondary byproduct of selection for some function unrelated to forceful biting behaviors. These results are consistent with the hypothesis that a shift to softer foods and/or the innovation of pre-oral food processing techniques relaxed selective pressures maintaining craniofacial features that favor forceful biting and chewing behaviors, leading to the characteristically small and gracile faces of modern humans.

Dental abrasion as a cutting process.

A mammalian tooth is abraded when a sliding contact between a particle and the tooth surface leads to an immediate loss of tooth tissue. Over time, these contacts can lead to wear serious enough to impair the oral processing of food. Both anatomical and physiological mechanisms have evolved in mammals to try to prevent wear, indicating its evolutionary importance, but it is still an established survival threat. Here we consider that many wear marks result from a cutting action whereby the contacting tip(s) of such wear particles acts akin to a tool tip. Recent theoretical developments show that it is possible to estimate the toughness of abraded materials via cutting tests. Here, we report experiments intended to establish the wear resistance of enamel in terms of its toughness and how friction varies. Imaging via atomic force microscopy (AFM) was used to assess the damage involved. Damage ranged from pure plastic deformation to fracture with and without lateral microcracks. Grooves cut with a Berkovich diamond were the most consistent, suggesting that the toughness of enamel in cutting is 244 J m(-2), which is very high. Friction was higher in the presence of a polyphenolic compound, indicating that this could increase wear potential.

Mechanical evidence that Australopithecus sediba was limited in its ability to eat hard foods.

Australopithecus sediba has been hypothesized to be a close relative of the genus Homo. Here we show that MH1, the type specimen of A. sediba, was not optimized to produce high molar bite force and appears to have been limited in its ability to consume foods that were mechanically challenging to eat. Dental microwear data have previously been interpreted as indicating that A. sediba consumed hard foods, so our findings illustrate that mechanical data are essential if one aims to reconstruct a relatively complete picture of feeding adaptations in extinct hominins. An implication of our study is that the key to understanding the origin of Homo lies in understanding how environmental changes disrupted gracile australopith niches. Resulting selection pressures led to changes in diet and dietary adaption that set the stage for the emergence of our genus.