Callum F. Ross

Symphyseal fusion and jaw-adductor muscle force: an EMG study.

The purpose of this study is to test various hypotheses about balancing-side jaw muscle recruitment patterns during mastication, with a major focus on testing the hypothesis that symphyseal fusion in anthropoids is due mainly to vertically- and/or transversely-directed jaw muscle forces. Furthermore, as the balancing-side deep masseter has been shown to play an important role in wishboning of the macaque mandibular symphysis, we test the hypothesis that primates possessing a highly mobile mandibular symphysis do not exhibit the balancing-side deep masseter firing pattern that causes wishboning of the anthropoid mandible. Finally, we also test the hypothesis that balancing-side muscle recruitment patterns are importantly related to allometric constraints associated with the evolution of increasing body size. Electromyographic (EMG) activity of the left and right superficial and deep masseters were recorded and analyzed in baboons, macaques, owl monkeys, and thick-tailed galagos. The masseter was chosen for analysis because in the frontal projection its superficial portion exerts force primarily in the vertical (dorsoventral) direction, whereas its deep portion has a relatively larger component of force in the transverse direction. The symphyseal fusion-muscle recruitment hypothesis predicts that unlike anthropoids, galagos develop bite force with relatively little contribution from their balancing-side jaw muscles. Thus, compared to galagos, anthropoids recruit a larger percentage of force from their balancing-side muscles. If true, this means that during forceful mastication, galagos should have working-side/balancing-side (W/B) EMG ratios that are relatively large, whereas anthropoids should have W/B ratios that are relatively small. The EMG data indicate that galagos do indeed have the largest average W/B ratios for both the superficial and deep masseters (2.2 and 4.4, respectively). Among the anthropoids, the average W/B ratios for the superficial and deep masseters are 1.9 and 1.0 for baboons, 1.4 and 1.0 for macaques, and both values are 1.4 for owl monkeys. Of these ratios, however, the only significant difference between thick-tailed galagos and anthropoids are those associated with the deep masseter. Furthermore, the analysis of masseter firing patterns indicates that whereas baboons, macaques and owl monkeys exhibit the deep masseter firing pattern associated with wishboning of the macaque mandibular symphysis, galagos do not exhibit this firing pattern. The allometric constraint-muscle recruitment hypothesis predicts that larger primates must recruit relatively larger amounts of balancing-side muscle force so as to develop equivalent amounts of bite force. Operationally this means that during forceful mastication, the W/B EMG ratios for the superficial and deep masseters should be negatively correlated with body size. Our analysis clearly refutes this hypothesis. As already noted, the average W/B ratios for both the superficial and deep masseter are largest in thick-tailed galagos, and not, as predicted by the allometric constraint hypothesis, in owl monkeys, an anthropoid whose body size is smaller than that of thick-tailed galagos. Our analysis also indicates that owl monkeys have W/B ratios that are small and more similar to those of the much larger-sized baboons and macaques. Thus, both the analysis of the W/B EMG ratios and the muscle firing pattern data support the hypothesis that symphyseal fusion and transversely-directed muscle force in anthropoids are functionally linked. This in turn supports the hypothesis that the evolution of symphyseal fusion in anthropoids is an adaptation to strengthen the symphysis so as to counter increased wishboning stress during forceful unilateral mastication. (ABSTRACT TRUNCATED)

Mandibular corpus strain in primates: Further evidence for a functional link between symphyseal fusion and jaw‐adductor muscle force

Previous work indicates that compared to adult thick-tailed galagos, adult long-tailed macaques have much more bone strain on the balancing-side mandibular corpus during unilateral isometric molar biting (Hylander [1979a] J. Morphol. 159:253-296). Recently we have confirmed in these same two species the presence of similar differences in bone-strain patterns during forceful mastication. Moreover, we have also recorded mandibular bone strain patterns in adult owl monkeys, which are slightly smaller than the galago subjects. The owl monkey data indicate the presence of a strain pattern very similar to that recorded for macaques, and quite unlike that recorded for galagos. We interpret these bone-strain pattern differences to be importantly related to differences in balancing-side jaw-adductor muscle force recruitment patterns. That is, compared to galagos, macaques and owl monkeys recruit relatively more balancing-side jaw-adductor muscle force during forceful mastication. Unlike an earlier study (Hylander [1979b] J. Morphol. 160:223-240), we are unable to estimate the actual amount of working-side muscle force relative to balancing-side muscle force (i.e., the W/B muscle force ratio) in these species because we have no reliable estimate of magnitude, direction, and precise location of the bite force during mastication. A comparison of the mastication data with the earlier data recorded during isometric molar biting, however, supports the hypothesis that the two anthropoids have a small W/B jaw-adductor muscle force ratio in comparison to thick-tailed galagos. These data also support the hypothesis that increased recruitment of balancing-side jaw-adductor muscle force in anthropoids is functionally linked to the evolution of symphyseal fusion or strengthening. Moreover, these data refute the hypothesis that the recruitment pattern differences between macaques and thick-tailed galagos are due to allometric factors. Finally, although the evolution of symphyseal fusion in primates may be linked to increased stress associated with increased balancing-side muscle force, it is currently unclear as to whether the increased force is predominately vertically directed, transversely directed, or is a near equal combination of these two force components (cf. Ravosa and Hylander [1994] In Fleagle and Kay [eds.]: Anthropoid Origins. New York: Plenum, pp. 447-468).

Effects of brain and facial size on basicranial form in human and primate evolution

Understanding variation in the basicranium is of central importance to paleoanthropology because of its fundamental structural role in skull development and evolution. Among primates, encephalisation is well known to be associated with flexion between midline basicranial elements, although it has been proposed that the size or shape of the face influences basicranial flexion. In particular, brain size and facial size are hypothesized to act as antagonists on basicranial flexion. One important and unresolved problem in hominin skull evolution is that large-brained Neanderthals and some Mid-Pleistocene humans have slightly less flexed basicrania than equally large-brained modern humans. To determine whether or not this is a consequence of differences in facial size, geometric morphometric methods were applied to a large comparative data set of non-human primates, hominin fossils, and humans (N=142; 29 species). Multiple multivariate regression and thin plate spline analyses suggest that basicranial evolution is highly significantly influenced by both brain size and facial size. Increasing facial size rotates the basicranium away from the face and slightly increases the basicranial angle, whereas increasing brain size reduces the angles between the spheno-occipital clivus and the presphenoid plane, as well as between the latter and the cribriform plate. These interactions can explain why Neanderthals and some Mid-Pleistocene humans have less flexed cranial bases than modern humans, despite their relatively similar brain sizes. We highlight that, in addition to brain size (the prime factor implicated in basicranial evolution in Homo), facial size is an important influence on basicranial morphology and orientation. To better address the multifactorial nature of basicranial flexion, future studies should focus on the underlying factors influencing facial size evolution in hominins.

Adaptive explanation for the origins of the anthropoidea (primates)

A new explanation for the origin of the primate suborder Anthropoidea is presented. Functional analyses of the “forward”‐facing orbits, postorbital septum and retinal fovea are used to reconstruct the morphological and ecological contexts in which these features are most likely to have evolved. The postorbital septum is argued to have evolved as an adaptation to protect the orbital contents from encroaching fibers of anterior temporalis. This encroachment resulted from increasing convergence and frontation of the orbital margins in a lineage of small‐bodied animals with relatively large eyes. Increasing orbital convergence is hypothesized to have resulted from reduction in relative orbit diameter associated with a shift to diurnality at small body size (<1,300 g). Increased frontation (verticality) of the orbital margins is hypothesized to have been due to rostral displacement of the superior orbital margin or increasing basicranial flexion in a lineage of animals with orbits pushed to the midline below the olfactory tract. Either of these changes would have occurred as a result of increases in neocortex size. Increased neocortical volume is hypothesized to have resulted from a shift to group living associated with a shift to diurnality. Diurnal, visual predation among other vertebrates is commonly associated with possession of a retinal fovea and the haplorhine fovea is hypothesized to have evolved in a similar context. All these features are hypothesized to have evolved in association with a shift from nocturnal to diurnal visual predation of insects at small body size and this adaptive shift is argued to be the defining feature of the anthropoid suborder. The omomyid skull is the best structural antecedent of the anthropoid skull; however, if basal primates exhibited moderate degrees of orbital convergence and frontation, orbits that were closely approximated below the olfactory tract and nocturnal habits, they could easily have given rise to the anthropoid stem species. The presence of a retinal fovea and lack of a tapetum lucidum in extant tarsiers implies that they shared a diurnal ancestry with anthropoids. This suggests that the adaptive explanation for anthropoid origins presented here applies to the origins of the haplorhine stem lineage.

Anthropoid origins : a phylogenetic analysis

Living Anthropoidea—the group that includes monkeys, apes, and humans—has long been recognized as a monophyletic group among primates diagnosed by a suite of features of the skull, dentition, and postcranium. Likewise it is agreed that there are two monophyletic groups of living anthropoids—the Central and South American Platyrrhini (New World monkeys) and African and Eurasian Catarrhini (Old World monkeys, “apes,” and humans). As well, most paleontologists and neontologists agree that Tarsius is the closest living relative of anthropoids and that strepsirrhines, lemurs and lorises, are more distantly related (but see Eizirik et al., this volume for a different view). Paleontologists also generally accept the following “facts”: The oldest Tarsius relatives occur in the Asian middle Eocene. The oldest undisputed fossil record of anthropoids is from the late Eocene localities in Afro-Arabia. Platyrrhines first appear in the late Oligocene in South America and the catarrhine record is acknowledged by all to include Propliopithecidae from the early Oligocene of Egypt and Oman.

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.

The Craniofacial Evidence for Anthropoid and Tarsier Relationships

Monkeys and apes have long been observed to resemble humans in the external appearance of the head, having a globular braincase, a short snout, and forward-facing eyes. In 1864, Mivart grouped them in the suborder, Anthro-poidea, distinct from the Lemuroidea, to which he assigned lemurs, lorises, galagos, aye-ayes, and tarsiers (Mivart, 1864, p. 635). Although Mivart later (1873) identified a lengthy list of features distinguishing anthropoids from lemuroids, he maintained that New and Old World anthropoids had evolved in parallel from separate nonprimate ancestors. Mivart’s conception of An-thropoidea—a polyphyletic taxon united by numerous distinctive features of the skull—thrived in the intellectual milieu of the “classical primatological synthesis” in which parallelism was seen as a widespread phenomenon (e.g., Le Gros Glark, 1934, 1959; Simpson, 1945, 196D. However, with the adoption by primate systematists of the principles of phylogenetic systematics (Hennig, 1966) and, later, of the parsimony criterion for choosing between competing hypotheses of evolutionary relationships, the assumption of widespread parallelism fell out of vogue. Anthropoids have come to be interpreted as a closed descent community (sensu Ax, 1985), and their distinctive features have been reinterpreted as synapomorphies inherited from an ancestral stem species.

Bone strain gradients and optimization in vertebrate skulls

It is often stated that the skull is optimally designed for resisting feeding forces, where optimality is defined as maximum strength with minimum material. Running counter to this hypothesis are bone strain gradients--variation in bone strain magnitudes across the skull--which in the primate skull have been hypothesized to suggest that different parts of the skull are optimized for different functions. In this paper strain gradients in the skulls of four genera of primates, Sus, and Alligator were documented and compared. Strain gradients were pervasive in all taxa sampled. Patterns of strain gradients showed inter-taxon differences, but strains in the mandible and zygomatic arch were always higher than those in the circumorbital and neurocranial regions. Strain magnitudes in Alligator were twice as high as those in mammals. Strain gradients were also positively allometric; i. e., larger primates show steeper gradients (larger differences) between the mandible and circumorbital region than smaller primates. Different strain magnitudes in different areas of the same animal are hypothesized to reflect optimization to different criteria. It is therefore hardly surprising that the skull, in which numerous functional systems are found, exhibits very steep gradients. Inter-specific differences in strain magnitudes at similar sites also suggest inter-specific differences in optimality criteria. The higher strain magnitudes in the Alligator skull suggest that the Alligator skull may be designed to experience extremely high strains less frequently whereas the primate skull may be designed to resist lower strains more frequently.

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. Anat Rec, 293:583–593, 2010.

Modulation of mandibular loading and bite force in mammals during mastication

SUMMARY Modulation of force during mammalian mastication provides insight into force modulation in rhythmic, cyclic behaviors. This study uses in vivo bone strain data from the mandibular corpus to test two hypotheses regarding bite force modulation during rhythmic mastication in mammals: (1) that bite force is modulated by varying the duration of force production, or (2) that bite force is modulated by varying the rate at which force is produced. The data sample consists of rosette strain data from 40 experiments on 11 species of mammals, including six primate genera and four nonprimate species: goats, pigs, horses and alpacas. Bivariate correlation and multiple regression methods are used to assess relationships between maximum (ϵ1) and minimum (ϵ2) principal strain magnitudes and the following variables: loading time and mean loading rate from 5% of peak to peak strain, unloading time and mean unloading rate from peak to 5% of peak strain, chew cycle duration, and chew duty factor. Bivariate correlations reveal that in the majority of experiments strain magnitudes are significantly (P<0.001) correlated with strain loading and unloading rates and not with strain loading and unloading times. In those cases when strain magnitudes are also correlated with loading times, strain magnitudes are more highly correlated with loading rate than loading time. Multiple regression analyses reveal that variation in strain magnitude is best explained by variation in loading rate. Loading time and related temporal variables (such as overall chew cycle time and chew duty factor) do not explain significant amounts of additional variance. Few and only weak correlations were found between strain magnitude and chew cycle time and chew duty factor. These data suggest that bite force modulation during rhythmic mastication in mammals is mainly achieved by modulating the rate at which force is generated within a chew cycle, and less so by varying temporal parameters. Rate modulation rather than time modulation may allow rhythmic mastication to proceed at a relatively constant frequency, simplifying motor control computation.)