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.

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.

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.

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.

Hominid mandibular corpus shape variation and its utility for recognizing species diversity within fossil Homo.

Mandibular corpora are well represented in the hominin fossil record, yet few studies have rigorously assessed the utility of mandibular corpus morphology for species recognition, particularly with respect to the linear dimensions that are most commonly available. In this study, we explored the extent to which commonly preserved mandibular corpus morphology can be used to: (i) discriminate among extant hominid taxa and (ii) support species designations among fossil specimens assigned to the genus Homo. In the first part of the study, discriminant analysis was used to test for significant differences in mandibular corpus shape at different taxonomic levels (genus, species and subspecies) among extant hominid taxa (i.e. Homo, Pan, Gorilla, Pongo). In the second part of the study, we examined shape variation among fossil mandibles assigned to Homo (including H. habilis sensu stricto, H. rudolfensis, early African H. erectus/H. ergaster, late African H. erectus, Asian H. erectus, H. heidelbergensis, H. neanderthalensis and H. sapiens). A novel randomization procedure designed for small samples (and using group 'distinctness values') was used to determine whether shape variation among the fossils is consistent with conventional taxonomy (or alternatively, whether a priori taxonomic groupings are completely random with respect to mandibular morphology). The randomization of 'distinctness values' was also used on the extant samples to assess the ability of the test to recognize known taxa. The discriminant analysis results demonstrated that, even for a relatively modest set of traditional mandibular corpus measurements, we can detect significant differences among extant hominids at the genus and species levels, and, in some cases, also at the subspecies level. Although the randomization of 'distinctness values' test is more conservative than discriminant analysis (based on comparisons with extant specimens), we were able to detect at least four distinct groups among the fossil specimens (i.e. H. sapiens, H. heidelbergensis, Asian H. erectus and a combined 'African Homo' group consisting of H. habilis sensu stricto, H. rudolfensis, early African H. erectus/H. ergaster and late African H. erectus). These four groups appear to be distinct at a level similar to, or greater than, that of modern hominid species. In addition, the mandibular corpora of H. neanderthalensis could be distinguished from those of 'African Homo', although not from those of H. sapiens, H. heidelbergensis, or the Asian H. erectus group. The results suggest that the features most commonly preserved on the hominin mandibular corpus have some taxonomic utility, although they are unlikely to be useful in generating a reliable alpha taxonomy for early African members of the genus Homo.

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.

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.

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.

Modeling masticatory muscle force in finite element analysis: sensitivity analysis using principal coordinates analysis.

Our work on a finite element model of the skull of Macaca aims to investigate the functional significance of specific features of primate skulls and to determine to which of the input variables (elastic properties, muscle forces) the model behavior is most sensitive. Estimates of muscle forces acting on the model are derived from estimates of physiological cross-sectional areas (PCSAs) of the jaw muscles scaled by relative electromyographic (EMG) amplitudes recorded in vivo. In this study, the behavior of the model was measured under different assumptions regarding the PCSAs of the jaw muscles and the latency between EMG activity in those muscles and the resulting force production. Thirty-six different loading regimes were applied to the model using four different PCSA sets and nine different PCSA scaling parameters. The four PCSA sets were derived from three different macaque species and one genus average, and the scaling parameters were either EMGs from 10, 20, 30, 40, 50 and 60 msec prior to peak bite force, or simply 100%, 50%, or 25% of peak muscle force. Principal coordinates analysis was used to compare the deformations of the model produced by the 36 loading regimes. Strain data from selected sites on the model were also compared with in vivo bone strain data. The results revealed that when varying the external muscle forces within these boundaries, the majority of the variation in model behavior is attributable to variation in the overall magnitude rather than the relative amount of muscle force generated by each muscle. Once this magnitude-related variation in model deformation was accounted for, significant variation was attributable to differences in relative muscle recruitment between working and balancing sides. Strain orientations at selected sites showed little variation across loading experiments compared with variation documented in vivo. These data suggest that in order to create an accurate and valid finite element model of the behavior of the primate skull at a particular instant during feeding, it is important to include estimates of the relative recruitment levels of the masticatory muscles. However, a lot can be learned about patterns of skull deformation, in fossil species for example, by applying external forces proportional to the estimated relative PCSAs of the jaw adductors.

Biomechanical implications of intraspecific shape variation in chimpanzee crania: moving toward an integration of geometric morphometrics and finite element analysis.

In a broad range of evolutionary studies, an understanding of intraspecific variation is needed in order to contextualize and interpret the meaning of variation between species. However, mechanical analyses of primate crania using experimental or modeling methods typically encounter logistical constraints that force them to rely on data gathered from only one or a few individuals. This results in a lack of knowledge concerning the mechanical significance of intraspecific shape variation that limits our ability to infer the significance of interspecific differences. This study uses geometric morphometric methods (GM) and finite element analysis (FEA) to examine the biomechanical implications of shape variation in chimpanzee crania, thereby providing a comparative context in which to interpret shape-related mechanical variation between hominin species. Six finite element models (FEMs) of chimpanzee crania were constructed from CT scans following shape-space Principal Component Analysis (PCA) of a matrix of 709 Procrustes coordinates (digitized onto 21 specimens) to identify the individuals at the extremes of the first three principal components. The FEMs were assigned the material properties of bone and were loaded and constrained to simulate maximal bites on the P(3) and M(2) . Resulting strains indicate that intraspecific cranial variation in morphology is associated with quantitatively high levels of variation in strain magnitudes, but qualitatively little variation in the distribution of strain concentrations. Thus, interspecific comparisons should include considerations of the spatial patterning of strains rather than focus only on their magnitudes.

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.

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.

The global impact of sutures assessed in a finite element model of a macaque cranium.

The biomechanical significance of cranial sutures in primates is an open question because their global impact is unclear, and their material properties are difficult to measure. In this study, eight suture-bone functional units representing eight facial sutures were created in a finite element model of a monkey cranium. All the sutures were assumed to have identical isotropic linear elastic material behavior that varied in different modeling experiments, representing either fused or unfused sutures. The values of elastic moduli employed in these trials ranged over several orders of magnitude. Each model was evaluated under incisor, premolar, and molar biting conditions. Results demonstrate that skulls with unfused sutures permitted more deformations and experienced higher total strain energy. However, strain patterns remained relatively unaffected away from the suture sites, and bite reaction force was likewise barely affected. These findings suggest that suture elasticity does not substantially alter load paths through the macaque skull or its underlying rigid body kinematics. An implication is that, for the purposes of finite element analysis, omitting or fusing sutures is a reasonable modeling approximation for skulls with small suture volume fraction if the research objective is to observe general patterns of craniofacial biomechanics under static loading conditions. The manner in which suture morphology and ossification affect the mechanical integrity of skulls and their ontogeny and evolution awaits further investigation, and their viscoelastic properties call for dynamic simulations.

The structural rigidity of the cranium of Australopithecus africanus: implications for diet, dietary adaptations, and the allometry of feeding biomechanics.

Australopithecus africanus is an early hominin (i.e., human relative) believed to exhibit stress-reducing adaptations in its craniofacial skeleton that may be related to the consumption of resistant food items using its premolar teeth. Finite element analyses simulating molar and premolar biting were used to test the hypothesis that the cranium of A. africanus is structurally more rigid than that of Macaca fascicularis, an Old World monkey that lacks derived australopith facial features. Previously generated finite element models of crania of these species were subjected to isometrically scaled loads, permitting a direct comparison of strain magnitudes. Moreover, strain energy (SE) in the models was compared after results were scaled to account for differences in bone volume and muscle forces. Results indicate that strains in certain skeletal regions below the orbits are higher in M. fascicularis than in A. africanus. Moreover, although premolar bites produce von Mises strains in the rostrum that are elevated relative to those produced by molar biting in both species, rostral strains are much higher in the macaque than in the australopith. These data suggest that at least the midface of A. africanus is more rigid than that of M. fascicularis. Comparisons of SE reveal that the A. africanus cranium is, overall, more rigid than that of M. fascicularis during premolar biting. This is consistent with the hypothesis that this hominin may have periodically consumed large, hard food items. However, the SE data suggest that the A. africanus cranium is marginally less rigid than that of the macaque during molar biting. It is hypothesized that the SE results are being influenced by the allometric scaling of cranial cortical bone thickness.

Masticatory biomechanics and its relevance to early hominid phylogeny: an examination of palatal thickness using finite-element analysis.

It has been proposed that morphological characters functionally related to mastication may be unreliable indicators of early hominid phylogeny. One hypothesis states that masticatory characters are highly prone to homoplasy. A second hypothesis states that such characters are likely to be morphologically integrated and thus violate the assumption of character independence implicit in all phylogenetic analyses. Evaluation of these hypotheses requires that masticatory features be accurately identified, but, to date, there have been relatively few attempts to test precisely which early hominid features are functionally related to chewing. This paper uses finite-element analysis to evaluate the functional relationships of a character--palatal thickness--that is one of several Paranthropus synapomorphies putatively related to mastication. A finite-element model of 145,680 elements was created from sixty-one 2-mm-thick CT scans of a Macaca fascicularis skull. The model was assigned the elastic properties of facial bone and loaded with muscle forces corresponding to the moment of centric occlusion during mastication. The model was constrained so as to produce a reaction force (corresponding to the bite force) at M(1). With a few exceptions, the strain patterns in the finite-element model compare well with those gathered from published and unpublished bone-strain experiments. The model was then modified to have a thick palate. The model was reloaded using an identical loading regime, and the strain patterns of the original and thick-palate models were compared. Although a thickened palate acts to reduce palatal strain, strains are elevated in other facial regions. This suggests that a thick palate would not have evolved in isolation as an adaptation to withstand masticatory stress. Rather, a thick palate may have evolved in concert with a suite of other facial features that share a stress-resistance function. This appears to be consistent with hypotheses positing that at least some facial features related to chewing evolved in an integrated fashion. More functional studies of other facial features are needed, as are formal studies of morphological integration.