Michael A. Berthaume

In vivo bone strain and finite-element modeling of the craniofacial haft in catarrhine primates.

Hypotheses regarding patterns of stress, strain and deformation in the craniofacial skeleton are central to adaptive explanations for the evolution of primate craniofacial form. The complexity of craniofacial skeletal morphology makes it difficult to evaluate these hypotheses with in vivo bone strain data. In this paper, new in vivo bone strain data from the intraorbital surfaces of the supraorbital torus, postorbital bar and postorbital septum, the anterior surface of the postorbital bar, and the anterior root of the zygoma are combined with published data from the supraorbital region and zygomatic arch to evaluate the validity of a finite‐element model (FEM) of a macaque cranium during mastication. The behavior of this model is then used to test hypotheses regarding the overall deformation regime in the craniofacial haft of macaques. This FEM constitutes a hypothesis regarding deformation of the facial skeleton during mastication. A simplified verbal description of the deformation regime in the macaque FEM is as follows. Inferior bending and twisting of the zygomatic arches about a rostrocaudal axis exerts inferolaterally directed tensile forces on the lateral orbital wall, bending the wall and the supraorbital torus in frontal planes and bending and shearing the infraorbital region and anterior zygoma root in frontal planes. Similar deformation regimes also characterize the crania of Homo and Gorilla under in vitro loading conditions and may be shared among extant catarrhines. Relatively high strain magnitudes in the anterior root of the zygoma suggest that the morphology of this region may be important for resisting forces generated during feeding.

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 Feeding Biomechanics and Dietary Ecology of Paranthropus boisei

The African Plio‐Pleistocene hominins known as australopiths evolved derived craniodental features frequently interpreted as adaptations for feeding on either hard, or compliant/tough foods. Among australopiths, Paranthropus boisei is the most robust form, exhibiting traits traditionally hypothesized to produce high bite forces efficiently and strengthen the face against feeding stresses. However, recent mechanical analyses imply that P. boisei may not have been an efficient producer of bite force and that robust morphology in primates is not necessarily strong. Here we use an engineering method, finite element analysis, to show that the facial skeleton of P. boisei is structurally strong, exhibits a strain pattern different from that in chimpanzees (Pan troglodytes) and Australopithecus africanus, and efficiently produces high bite force. It has been suggested that P. boisei consumed a diet of compliant/tough foods like grass blades and sedge pith. However, the blunt occlusal topography of this and other species suggests that australopiths are adapted to consume hard foods, perhaps including grass and sedge seeds. A consideration of evolutionary trends in morphology relating to feeding mechanics suggests that food processing behaviors in gracile australopiths evidently were disrupted by environmental change, perhaps contributing to the eventual evolution of Homo and Paranthropus. Anat Rec, 298:145–167, 2015.

The effect of early hominin occlusal morphology on the fracturing of hard food items.

Tooth profile plays an important role in interpretations of the functional morphology of extinct species. We tested hypotheses that australopith occlusal morphology influences the fracture force required to crack large, hard food items using a combination of physical testing and finite element analysis (FEA). We performed mechanical experiments simulating both molar and premolar biting using metal replicas of four hominin specimens representing species that differ in occlusal relief (Praeanthropus afarensis, Australopithecus africanus, Paranthropus robustus, and P. boisei). The replicas were inserted into an Instron machine and used to fracture hollow acrylic hemispheres with known material properties. These hemispheres simulate a hard and brittle food item but exhibit far less variability in size and strength than actual nuts or seeds, thereby facilitating interpretations of tooth function. Fracture forces and fracture displacements were measured, and analysis of variance revealed significant differences in fracture force and energy between specimens and tooth types. Complementing the physical testing, a nonlinear contact finite element model was developed to simulate each physical test. Experimental and FEA results showed good correspondence in most cases, and FEA identified stress concentrations consistent with mechanical models predicting that radial/median fractures are important factors in the failure of nut and seed shells. The fracture force data revealed functional similarities between relatively unworn Pr. afarensis and P. robustus teeth, and between relatively unworn A. africanus and heavily worn P. boisei teeth. These results are inconsistent with functional hypotheses, and raise the possibility that the tooth morphology of early hominins and other hard object feeders may not represent adaptations for inducing fractures in large, hard food items, but rather for resisting fractures in the tooth crown. Anat Rec, 293:594–606, 2010.

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.

How does tooth cusp radius of curvature affect brittle food item processing

Tooth cusp sharpness, measured by radius of curvature (RoC), has been predicted to play a significant role in brittle/hard food item fracture. Here, we set out to test three existing hypotheses about this relationship: namely, the Blunt and Strong Cusp hypotheses, which predict that dull cusps will be most efficient at brittle food item fracture, and the Pointed Cusp hypothesis, which predicts that sharp cusps will be most efficient at brittle food item fracture using a four cusp bunodont molar. We also put forth and test the newly constructed Complex Cusp hypothesis, which predicts that a mixture of dull and sharp cusps will be most efficient at brittle food item fracture. We tested the four hypotheses using finite-element models of four cusped, bunodont molars. When testing the three existing hypotheses, we assumed all cusps had the same level of sharpness (RoC), and gained partial support for the Blunt Cusp hypotheses. We found no support for the Pointed Cusp or Strong Cusp hypotheses. We used the Taguchi sampling method to test the Complex Cusps hypothesis with a morphospace created by independently varying the radii of curvature of the four cusps in the buccolingual and mesiodistal directions. The optimal occlusal morphology for fracturing brittle food items consists of a combination of sharp and dull cusps, which creates high stress concentrations in the food item while stabilizing the food item and keeping the stress concentrations in the enamel low. This model performed better than the Blunt Cusp hypothesis, suggesting a role for optimality in the evolution of cusp form.

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.

Functional Implications of Squamosal Suture Size in Paranthropus boisei

It has been hypothesized that the extensively overlapping temporal and parietal bones of the squamosal sutures in Paranthropus boisei are adaptations for withstanding loads associated with feeding. Finite element analysis (FEA) was used to investigate the biomechanical effects of suture size (i.e., the area of overlap between the temporal and parietal bones) on stress, strain energy, and strain ratio in the squamosal sutures of Pan troglodytes and P. boisei (specimen OH 5) during biting. Finite element models (FEMs) of OH 5 and a P. troglodytes cranium were constructed from CT scans. These models contain sutures that approximate the actual suture sizes preserved in both crania. The FEM of Pan was then modified to create two additional FEMs with squamosal sutures that are 50% smaller and 25% larger than those in the original model. Comparisons among the models test the effect of suture size on the structural integrity of the squamosal suture as the temporal squama and parietal bone move relative to each other during simulated premolar biting. Results indicate that with increasing suture size there is a decreased risk of suture failure, and that maximum stress values in the OH 5 suture were favorable compared to values in the Pan model with the normal suture size. Strain ratios suggest that shear is an important strain regime in the squamosal suture. This study is consistent with the hypothesis that larger sutures help reduce the likelihood of suture failure under high biting loads.

Tooth cusp sharpness as a dietary correlate in great apes

Mammalian molars have undergone heavy scrutiny to determine correlates between morphology and diet. Here, the relationship between one aspect of occlusal morphology, tooth cusp radius of curvature (RoC), and two broad dietary categories, folivory and frugivory, is analyzed in apes. The author hypothesizes that there is a relationship between tooth cusp RoC and diet, and that folivores have sharper teeth than frugivores, and further test the correlation between tooth cusp RoC and tooth cusp size. Eight measures of tooth cusp RoC (two RoCs per cusp) were taken from 53 M(2) s from four species and subspecies of frugivorous apes (Pongo pygmaeus, Pan troglodytes troglodytes, Pan troglodytes schweinfurthii, and Gorilla gorilla gorilla) and two subspecies of folivorous apes (Gorilla beringei beringei, and Gorilla beringei graueri). Phylogenetically corrected ANOVAs were run on the full dataset and several subsets of the full dataset, revealing that, when buccolingual RoCs are taken into account, tooth cusp RoCs can successfully differentiate folivores and frugivores. PCAs revealed that folivores consistently had duller teeth than frugivores. In addition, a weak, statistically significant positive correlation exists between tooth cusp size and tooth cusp RoC. The author hypothesizes differences in tooth cusp RoC are correlated with wear rates, where, per vertical unit of wear, duller cusps will have a longer length of exposed enamel ridge than sharper cusps. More data need to be gathered to determine if the correlation between tooth cusp RoC and tooth cusp size holds true when small primates are considered.

The effects of relative food item size on optimal tooth cusp sharpness during brittle food item processing

Teeth are often assumed to be optimal for their function, which allows researchers to derive dietary signatures from tooth shape. Most tooth shape analyses normalize for tooth size, potentially masking the relationship between relative food item size and tooth shape. Here, we model how relative food item size may affect optimal tooth cusp radius of curvature (RoC) during the fracture of brittle food items using a parametric finite-element (FE) model of a four-cusped molar. Morphospaces were created for four different food item sizes by altering cusp RoCs to determine whether optimal tooth shape changed as food item size changed. The morphospaces were also used to investigate whether variation in efficiency metrics (i.e. stresses, energy and optimality) changed as food item size changed. We found that optimal tooth shape changed as food item size changed, but that all optimal morphologies were similar, with one dull cusp that promoted high stresses in the food item and three cusps that acted to stabilize the food item. There were also positive relationships between food item size and the coefficients of variation for stresses in food item and optimality, and negative relationships between food item size and the coefficients of variation for stresses in the enamel and strain energy absorbed by the food item. These results suggest that relative food item size may play a role in selecting for optimal tooth shape, and the magnitude of these selective forces may change depending on food item size and which efficiency metric is being selected.