Masseter electromyography during chewing in ring-tailed lemurs (Lemur catta)

We examined masseter recruitment and firing patterns during chewing in four adult ring-tailed lemurs (Lemur catta), using electromyography (EMG). During chewing of tougher foods, the working-side superficial masseter tends to show, on average, 1.7 times more scaled EMG activity than the balancing-side superficial masseter. The working-side deep masseter exhibits, on average, 2.4 times the scaled EMG activity of the balancing-side deep masseter. The relatively larger activity in the working-side muscles suggests that ring-tailed lemurs recruit relatively less force from their balancing-side muscles during chewing. The superficial masseter working-to-balancing-side (W/B) ratio for lemurs overlaps with W/B ratios from anthropoid primates. In contrast, the lemur W/B ratio for the deep masseter is more similar to that of greater galagos, while both are significantly larger than W/B ratios of anthropoids. Because ring-tailed lemurs have unfused and hence presumably weaker symphyses, these data are consistent with the symphyseal fusion-muscle recruitment hypothesis stating that symphyseal fusion in anthropoids provides increased strength for resisting forces created by the balancing-side jaw muscles during chewing. Among the masseter muscles of ring-tailed lemurs, the working-side deep masseter peaks first on average, followed in succession by the balancing-side deep masseter, balancing-side superficial masseter, and finally the working-side superficial masseter. Ring-tailed lemurs are similar to greater galagos in that their balancing-side deep masseter peaks well before their working-side superficial masseter. We see the opposite pattern in anthropoids, where the balancing-side deep masseter peaks, on average, after the working-side superficial masseter. This late activity of the balancing-side deep masseter in anthropoids is linked to lateral-transverse bending, or wishboning, of their mandibular symphyses. Subsequently, the stresses incurred during wishboning are hypothesized to be a proximate reason for strengthening, and hence fusion, of the anthropoid symphysis. Thus, the absence of this muscle-firing pattern in ring-tailed lemurs with their weaker, unfused symphyses provides further correlational support for the symphyseal fusion late-acting balancing-side deep masseter hypothesis linking wishboning and symphyseal strengthening in anthropoids. The early peak activity of the working-side deep masseter in ring-tailed lemurs is unlike galagos and most similar to the pattern seen in macaques and baboons. We hypothesize that this early activity of the working-side deep masseter moves the lower jaw both laterally toward the working side and vertically upward, to position it for the upcoming power stroke. From an evolutionary perspective, the differences in peak firing times for the working-side deep masseter between ring-tailed lemurs and greater galagos indicate that deep masseter firing patterns are not conserved among strepsirrhines.     

Temporalis function in anthropoids and strepsirrhines: an EMG study

The major purpose of this study is to analyze anterior and posterior temporalis muscle force recruitment and firing patterns in various anthropoid and strepsirrhine primates. There are two specific goals for this project. First, we test the hypothesis that in addition to transversely directed muscle force, the evolution of symphyseal fusion in primates may also be linked to vertically directed balancing-side muscle force during chewing (Hylander et al. [2000] Am. J. Phys. Anthropol. 112:469-492). Second, we test the hypothesis of whether strepsirrhines retain the hypothesized primitive mammalian condition for the firing of the anterior temporalis, whereas anthropoids have the derived condition (Weijs [1994] Biomechanics of Feeding in Vertebrates; Berlin: Springer-Verlag, p. 282-320). Electromyographic (EMG) activities of the left and right anterior and posterior temporalis muscles were recorded and analyzed in baboons, macaques, owl monkeys, thick-tailed galagos, and ring-tailed lemurs. In addition, as we used the working-side superficial masseter as a reference muscle, we also recorded and analyzed EMG activity of the left and right superficial masseter in these primates. The data for the anterior temporalis provided no support for the hypothesis that symphyseal fusion in primates is linked to vertically directed jaw muscle forces during mastication. Thus, symphyseal fusion in primates is most likely mainly linked to the timing and recruitment of transversely directed forces from the balancing-side deep masseter (Hylander et al. [2000] Am. J. Phys. Anthropol. 112:469-492). In addition, our data demonstrate that the firing patterns for the working- and balancing-side anterior temporalis muscles are near identical in both strepsirrhines and anthropoids. Their working- and balancing-side anterior temporalis muscles fire asynchronously and reach peak activity during the power stroke. Similarly, their working- and balancing-side posterior temporalis muscles also fire asynchronously and reach peak activity during the power stroke. Compared to these strepsirrhines, however, the balancing-side posterior temporalis of anthropoids appears to have a relatively delayed firing pattern. Moreover, based on their smaller W/B ratios, anthropoids demonstrate a relative increase in muscle-force recruitment of the balancing-side posterior temporalis. This in turn suggests that anthropoids may emphasize the duration and magnitude of the power stroke during mastication. This hypothesis, however, requires additional testing. Furthermore, during the latter portion of the power stroke, the late activity of the balancing-side posterior temporalis of anthropoids apparently assists the balancing-side deep masseter in driving the working-side molars through the terminal portion of occlusion.     

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)     

Jaw-muscle electromyography during chewing in Belanger's treeshrews (Tupaia belangeri)

We examined masseter and temporalis recruitment and firing patterns during chewing in five male Belanger's treeshrews (Tupaia belangeri), using electromyography (EMG). During chewing, the working-side masseters tend to show almost three times more scaled EMG activity than the balancing-side masseters. Similarly, the working-side temporalis muscles have more than twice the scaled EMG activity of the balancing-side temporalis. The relatively higher activity in the working-side muscles suggests that treeshrews recruit less force from their balancing-side muscles during chewing. Most of the jaw-closing muscles in treeshrews can be sorted into an early-firing or late-firing group, based on occurrence of peak activity during the chewing cycle. Specifically, the first group of jaw-closing muscles to reach peak activity consists of the working-side anterior and posterior temporalis and the balancing-side superficial masseter. The balancing-side anterior and posterior temporalis and the working-side superficial masseter peak later in the power stroke. The working-side deep masseter peaks, on average, slightly before the working-side superficial masseter. The balancing-side deep masseter typically peaks early, at about the same time as the balancing-side superficial masseter. Thus, treeshrews are unlike nonhuman anthropoids that peak their working-side deep masseters early and their balancing-side deep masseters late in the power stroke. Because in anthropoids the late firing of the balancing-side deep masseter contributes to wishboning of the symphysis, the treeshrew EMG data suggest that treeshrews do not routinely wishbone their symphyses during chewing. Based on the treeshrew EMG data, we speculate that during chewing, primitive euprimates 1) recruited more force from the working-side jaw-closing muscles as compared to the balancing-side muscles, 2) fired an early group of jaw-closing muscles followed by a second group of muscles that peaked later in the power stroke, 3) did not fire their working-side deep masseter significantly earlier than their working-side superficial masseter, and 4) did not routinely fire their balancing-side deep masseter after the working-side superficial masseter.     

Mandibular form and function in North American and European Adapidae and Omomyidae

Previous experimental and comparative studies among a wide variety of primate and nonprimate mammals provide a unique source of information for investigating the functional and phylogenetic significance of variation in the masticatory apparatus of Eocene primates. To provide a quantitative study of mandibular form and function in Eocene primates, the scaling of jaw dimensions and the development of symphyseal fusion was considered in a broad sample of North American and European Adapidae and Omomyidae. Statistical analyses indicate a significant size-related pattern of symphyseal fusion across Eocene primates, with larger taxa often having a greater degree of fusion than smaller species; this trend is also evident at the family level. As adapids are mostly larger than omomyids and these taxa show allometry of symphyseal fusion, this may explain why no omomyids evince complete fusion. Controlling for jaw size, species with greater symphyseal fusion tend to have more robust jaws than those with a lesser amount of fusion. Upon further examination, a primary reason why adapids have more robust mandibles than omomyids is associated with the presence of taxa with fused symphyses, and thus more robust jaws, in the adapid sample, whereas no omomyids have fused symphyses. In addition, there is little indication of a dietary effect, as measured by molar shear-crest development, on symphyseal fusion. Moreover, as there is no correlation between molar shear-crest development and skull size, this also points to the absence of a size-related pattern of dietary preference underlying the allometry of symphyseal fusion. Based on the interspecific and ontogenetic allometry of symphyseal ossification in Eocene primates, jaw-scaling patterns are used to further examine the functional determinants of fusion in this group. This study indicates that greater dorsoventral shear during mastication is a more likely factor than lateral transverse bending (“wishboning”) in the evolution of symphyseal fusion among “late-fusing” mammals like adapids and omomyids. Given that wishboning is an important functional determinant of symphyseal form in recent anthropoids, apparently the evolutionary development of marked wishboning occurs only in taxa that shift the timing of fusion to a growth stage preceding the onset of weaning (before adult masticatory patterns are fully developed) and perhaps first ossified the symphysis to counter elevated dorsoventral shear stress. As early anthropoids probably consisted of members varying interspecifically and ontogenetically in the degree of ossification, it is especially informative to analyze the adaptive setting in which anthropoid symphyseal fusion evolved from a similar primitive “prosimian” perspective. © 1996 Wiley-Liss, Inc.     

Why fuse the mandibular symphysis? A comparative analysis

Fused symphyses, which evolved independently in several mammalian taxa, including anthropoids, are stiffer and stronger than unfused symphyses. This paper tests the hypothesis that orientations of tooth movements during occlusion are the primary basis for variations in symphyseal fusion. Mammals whose teeth have primarily dorsally oriented occlusal trajectories and/or rotate their mandibles during occlusion will not benefit from symphyseal fusion because it prevents independent mandibular movements and because unfused symphyses transfer dorsally oriented forces with equal efficiency; mammals with predominantly transverse power strokes are predicted to benefit from symphyseal fusion or greatly restricted mediolateral movement at the symphysis in order to increase force transfer efficiency across the symphysis in the transverse plane. These hypotheses are tested with comparative data on symphyseal and occlusal morphology in several mammals, and with kinematic and EMG analyses of mastication in opossums (Didelphis virginiana) and goats (Capra hircus) that are compared with published data on chewing in primates. Among mammals, symphyseal fusion or a morphology that greatly restricts movement correlates significantly with occlusal orientation: species with more transversely oriented occlusal planes tend to have fused symphyses. The ratio of working- to balancing-side adductor muscle force in goats and opossums is close to 1:1, as in macaques, but goats and opossums have mandibles that rotate independently during occlusion, and have predominantly vertically oriented tooth movements during the power stroke. Symphyseal fusion is therefore most likely an adaptation for increasing the efficiency of transfer of transversely oriented occlusal forces in mammals whose mandibles do not rotate independently during the power stroke.     

Transverse masticatory movements, occlusal orientation, and symphyseal fusion in selenodont artiodactyls

Based on extensive experimental work on primates, two masticatory loading regimes have emerged as the likely determinants of mandibular symphyseal fusion-dorsoventral shear and lateral transverse bending (wishboning) (Ravosa and Hylander, 1994; Hylander et al., 1998, 2000). Recently, however, it has been argued that, rather than functioning to strengthen the symphysis during mastication, fusion serves to stiffen the symphyseal joint so as to facilitate increased transverse jaw movements during occlusion (Lieberman and Crompton, 2000). As part of this transverse stiffness model, it has been suggested that taxa with fused symphyses should also exhibit more horizontally oriented occlusal wear facets. Using a series of univariate and bivariate analyses, we test predictions of these three models in a sample of 44 species of selenodont artiodactyls. Consistent with the wishboning and transverse stiffness models, taxa with fused symphyses (camelids) have more horizontally oriented M(2) and M(2) occlusal wear facets, anteroposteriorly (AP) elongate symphyses, and relatively wider corpora. Contrary to the dorsoventral shear model, camelids do not have relatively deeper corpora (due to greater parasagittal bending). While taxa with ossified symphyses have relatively larger symphysis cross-sectional areas, this appears to be the byproduct of an increase in AP symphysis length due to greater lateral transverse bending of the mandible. Theoretical consideration of the biomechanics of mastication further suggests that strength, not stiffness, is the critical factor in determining symphyseal ossification. Thus, like anthropoid primates, fusion in selenodont artiodactyls appears to function in resisting increased wishboning stresses arising from an emphasis on transverse occlusal/mandibular movements and loads.     

A preliminary analysis of correlations between chewing motor patterns and mandibular morphology across mammals

The establishment of a publicly-accessible repository of physiological data on feeding in mammals, the Feeding Experiments End-user Database (FEED), along with improvements in reconstruction of mammalian phylogeny, significantly improves our ability to address long-standing questions about the evolution of mammalian feeding. In this study, we use comparative phylogenetic methods to examine correlations between jaw robusticity and both the relative recruitment and the relative time of peak activity for the superficial masseter, deep masseter, and temporalis muscles across 19 mammalian species from six orders. We find little evidence for a relationship between jaw robusticity and electromyographic (EMG) activity for either the superficial masseter or temporalis muscles across mammals. We hypothesize that future analyses may identify significant associations between these physiological and morphological variables within subgroups of mammals that share similar diets, feeding behaviors, and/or phylogenetic histories. Alternatively, the relative peak recruitment and timing of the balancing-side (i.e., non-chewing-side) deep masseter muscle (BDM) is significantly negatively correlated with the relative area of the mandibular symphysis across our mammalian sample. This relationship exists despite BDM activity being associated with different loading regimes in the symphyses of primates compared to ungulates, suggesting a basic association between magnitude of symphyseal loads and symphyseal area among these mammals. Because our sample primarily represents mammals that use significant transverse movements during chewing, future research should address whether the correlations between BDM activity and symphyseal morphology characterize all mammals or should be restricted to this "transverse chewing" group. Finally, the significant correlations observed in this study suggest that physiological parameters are an integrated and evolving component of feeding across mammals.     

Patterns of variation across primates in jaw-muscle electromyography during mastication

Biologists that study mammals continue to discuss the evolutionof and functional variation in jaw-muscle activity during chewing.A major barrier to addressing these issues is collecting sufficientin vivo data to adequately capture neuromuscular variation ina clade. We combine data on jaw-muscle electromyography (EMG)collected during mastication from 14 species of primates andone of treeshrews to assess patterns of neuromuscular variationin primates. All data were collected and analyzed using thesame methods. We examine the variance components for EMG parametersusing a nested ANOVA design across successive hierarchical factorsfrom chewing cycle through species for eight locations in themasseter and temporalis muscles. Variation in jaw-muscle EMGswas not distributed equally across hierarchical levels. Thetiming of peak EMG activity showed the largest variance componentsamong chewing cycles. Relative levels of recruitment of jawmuscles showed the largest variance components among chewingsequences and cycles. We attribute variation among chewing cyclesto (1) changes in food properties throughout the chewing sequence,(2) variation in bite location, and (3) the multiple ways jawmuscles can produce submaximal bite forces. We hypothesize thatvariation among chewing sequences is primarily related to variationin properties of food. The significant proportion of variationin EMGs potentially linked to food properties suggests thatexperimental biologists must pay close attention to foods givento research subjects in laboratory-based studies of feeding.The jaw muscles exhibit markedly different variance componentsamong species suggesting that primate jaw muscles have evolvedas distinct functional units. The balancing-side deep masseter(BDM) exhibits the most variation among species. This observationsupports previous hypotheses linking variation in the timingand activation of the BDM to symphyseal fusion in anthropoidprimates and in strepsirrhines with robust symphyses. The working-sideanterior temporalis shows a contrasting pattern with littlevariation in timing and relative activation across primates.The consistent recruitment of this muscle suggests that primateshave maintained their ability to produce vertical jaw movementsand force in contrast to the evolutionary changes in transverseocclusal forces driven by the varying patterns of activationin the BDM.     

Anthropoid origins and the modern symphysis

To highlight adaptive transformations in craniomandibular form during anthropoid origins, symphyseal character states and underlying masticatory loading regimes were investigated vis-à-vis shifts in diet and body size. A study of fossil anthropoids is possible because variation in symphyseal fusion is continuous and directly proportional to the amount of symphyseal stress and because such variation can be considered a series of discrete character states each with unique functional underpinnings. Using recent systematic renderings of Eocene and Oligocene taxa as a template with which to assess character evolution, this analysis indicates when, and in which clade(s), specific masticatory features became fixed and thus diagnostic. A general trend throughout early anthropoid evolution is for descendent taxa to be progressively larger than ancestral forms. Coupled with this pattern is the tendency for larger-bodied fossil anthropoids to have ingested tougher diets variably consisting of thick-coated, unripe fruits and/or leaves. Mastication of mechanically tougher foods entails greater repetitive loading of the mandible and requires relatively larger amounts of balancing-side muscle force, thus resulting in correspondingly greater symphyseal fusion due to elevated dorsoventral shear. With a single exception, these adaptive transformations characterize the evolutionary pathway leading both to parapithecines and a catarrhine:platyrrhine clade (crown anthropoids). While the ancestor of crown anthropoids would have possessed a body size, diet and masticatory adaptations similar to parapithecines, such a common suite of features evolved independently. Moreover, the evolution of an early-fusing symphysis and associated wishboning loading regime of catarrhines and platyrrhines is unique among all anthropoids. Lastly, the apparent lack of reversals in symphyseal fusion indicates the improbability of phylogenetic hypotheses in which a relationship is proposed between 'ancestral' taxa with a greater degree of symphyseal fusion and 'descendent' anthropoids with a lesser degree of ossification.     

Loading patterns and jaw movements during mastication in Macaca fascicularis: a bone-strain, electromyographic, and cineradiographic analysis

Rosette strain gage, electromyography (EMG), and cineradiographic techniques were used to analyze loading patterns and jaw movements during mastication in Macaca fascicularis. The cineradiographic data indicate that macaques generally swallow frequently throughout a chewing sequence, and these swallows are intercalated into a chewing cycle towards the end of a power stroke. The bone strain and jaw movement data indicate that during vigorous mastication the transition between fast close and the power stroke is correlated with a sharp increase in masticatory force, and they also show that in most instances the jaws of macaques are maximally loaded prior to maximum intercuspation, i.e. during phase I (buccal phase) occlusal movements. Moreover, these data indicate that loads during phase II (lingual phase) occlusal movements are ordinarily relatively small. The bone strain data also suggest that the duration of unloading of the jaw during the power stroke of mastication is largely a function of the relaxation time of the jaw adductors. This interpretation is based on the finding that the duration from 100% peak strain to 50% peak strain during unloading closely approximates the half-relaxation time of whole adductor jaw muscles of macaques. The EMG data of the masseter and medial pterygoid muscles have important implications for understanding both the biomechanics of the power stroke and the external forces responsible for the "wishboning" effect that takes place along the mandibular symphysis and corpus during the power stroke of mastication. Although both medial pterygoid muscles reach maximum EMG activity during the power stroke, the activity of the working-side medial pterygoid peaks after the balancing-side medial pterygoid. Associated with the simultaneous increase of force of the working-side medial pterygoid and the decrease of force of the balancing-side medial pterygoid is the persistently high level of EMG activity of the balancing-side deep masseter (posterior portion). This pattern is of considerable significance because the direction of force of both the working-side medial pterygoid and the balancing-side deep masseter are well aligned to aid in driving the working-side lower molars across the upper molars in the medial direction during unilateral mastication.(ABSTRACT TRUNCATED AT 400 WORDS)     

Mandibular growth and function in Archaeolemur

Ontogenetic changes in the morphology of the mandibular symphysis are described in Archaeolemur so as to infer the functional significance of symphyseal fusion in this subfossil Malagasy lemur. The first regions of the symphysis to show a more complex morphology were the lower and anterior borders of the joint and, to a lesser extent, the lingual borders of the superior and inferior transverse tori. During growth, these regions became increasingly rugose and encroached upon a centrally located, smooth, “oval” region, which may have been a principal pathway for neurovascular structures communicating with the unfused joint. In subadults, the symphysis was completely fused except for the lingual surface of the inferior transverse torus, where a patent suture and potential space were present between dentaries. Thus, in Archaeolemur there was an age- and size-related pattern of increased symphyseal ossification or fusion that was complete by adulthood. The morphology of the interlocking bony processes and the sequence of ossification in the symphysis suggest that increased dorsoventral shear stress during mastication was the most likely determinant of symphyseal fusion in Archaeolemur: The allometric pattern of greater symphyseal fusion may be linked to the presence of relatively greater dorsoventral shear in adults due to an increased recruitment of balancing-side jaw-muscle force. There is little indication that the symphysis of juvenile Archaeolemur was buttressed to resist forces associated with “wishboning” during mastication or vertical bending during incision. Our observations, as well as those of others, suggest that symphyseal fusion in primates occurs initially as a response to increased dorsoventral shear during mastication. Therefore, wishboning stress might only become a major determinant of symphyseal form and function in those taxa that develop a fused symphysis to counter increased dorsoventral shear. © 1994 Wiley-Liss, Inc.     

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). Am J Phys Anthropol 107:257-271, 1998. © 1998 Wiley-Liss, Inc.     

The adaptive significance of mandibular symphyseal fusion in mammals

The mandibular symphyseal joint is remarkably variable across major mammalian clades, ranging in adults from unfused (amphiarthrosis) to partially fused (synarthrosis) to completely ossified (synostosis). Experimental work conducted on primates suggests that greater ossification of the symphysis is a response to increased recruitment of the balancing-side (i.e. nonchewing side) jaw-adductor muscles during forceful unilateral biting and chewing, with increased fusion strengthening the symphysis against correspondingly elevated joint stresses. It is thus expected that species with diets composed primarily of foods that require high-magnitude bite forces and/or repetitive loading to process will be characterized by greater degrees of symphyseal ossification than species with relatively easy-to-process diets (i.e. food items typified by low toughness and/or low stiffness). However, comparative support for this idea is limited. We tested this hypothesis in four dietarily diverse mammalian clades characterized by variation in symphyseal fusion - the Strepsirrhini, Marsupialia, Feliformia, and Caniformia. We scored fusion in adult specimens of 292 species, assigned each to a dietary category based on literature accounts, and tested for an association between these two variables using Pagel's test for the correlated evolution of binary characters. Results indicate that greater fusion is associated with diets composed of resistant items in strepsirrhines, marsupials, and feliforms, providing some support for the hypothesis. However, no such relationship was detected in caniforms, suggesting that factors other than dietary mechanical properties influence symphyseal ossification. Future work should focus on such factors, as well as those that favour an unfused mandibular symphysis.     

Ontogeny,function, and scaling of the mandibular symphysis in papionin primates

In vivo study of mastication in adult cercopithecine primates demonstrates a link between mandibular symphyseal form and resistance to “wishboning,” or lateral transverse bending. Mechanical consideration of wishboning at the symphysis indicates exponentially higher stresses along the lingual surface with increasing symphyseal curvature. Lengthening the anteroposterior width of the symphysis acts to resist these higher loads. Interspecific adult cercopithecine allometries show that both symphyseal curvature and symphyseal width exhibit positive allometry relative to body mass. The experimental and allometric data support an hypothesis that the cercopithecine mandibular symphysis is designed to maintain functional equivalence—in this case dynamic strain similarity—in wishboning stress and strain magnitudes across adult cercopithecines. We test the hypothesis that functional equivalence during masticatory wishboning is maintained throughout ontogeny by calculating relative stress estimates from morphometric dimensions of the mandibular symphysis in two cercopithecine primates, Macaca fascicularis and M. nemestrina. Results indicate no significant differences in relative stress estimates among the two macaque ontogenies and an interspecific sample of adult papionin primates. Further, relative stress estimates do not change significantly throughout ontogeny in either species. These results offer the first evidence for the maintenance of functional equivalence in stress and strain levels during postnatal growth in a habitually loaded cranial structure. Scaling analyses demonstrate significant slope differences for both symphyseal curvature and width between the ontogenetic and interspecific samples. The distinct interspecific cercopithecine slopes are realized by a series of ontogenetic transpositions in both symphyseal curvature and width. Throughout papionin ontogeny, symphyseal curvature increases with less negative allometry, while symphysis width increases with less positive allometry versus the interspecific pattern. As symphyseal curvature and width are inversely proportional to one another in estimating relative stresses, functionally equivalent stress levels are maintained both ontogenetically and interspecifically, because the relatively slower rate of allometric increase in symphyseal curvature during growth is compensated for by a slower rate of allometric increase in symphyseal width. These results indicate the primacy of maintaining functional equivalence during growth and the need for ontogenetic data in understanding the evolutionary processes that affect form–function relations as well as the interspecific patterning of adult form across a clade. J. Morphol. 235:157–175, 1998. © 1998 Wiley-Liss, Inc.     

Ontogeny of histochemical fiber types and muscle function in the masseter muscle of miniature swine

In this study of masticatory maturation, the ontogeny of the histochemical fiber type composition of musculus masseter is examined in the omnivorous miniature swine (Sus scrofa). Fiber type characteristics are interpreted by comparison with electromyography (EMG) recorded during feeding behavior. Similar to locomotion studies, the results suggest a correspondence between the composition and arrangement of motor units and their recruitment pattern. Serial sections of masseter muscles from 10 minipigs, ranging from 2 weeks to slightly over 1 year of age, were stained for myosin adenosine triphosphatase (mATPase) activity to distinguish slow-twitch from fast-twitch fibers, and for nicotinamide adenosine dehydrogenase-tetrazolium reductase to assess the aerobic capacity of the same fibers. Although maintaining a uniformly high aerobic capacity throughout ontogeny and in adult animals, a transition is observed in the relative proportions of fast- and slow-twitch fibers. The primarily fast-twitch neonatal pig masseter eventually comprises approximately 25-30% slow-twitch fibers in adults, with a higher predominance of slow fibers in the deep (vs. superficial) and anterior (vs. posterior) regions of the muscle. Furthermore, while individual fibers of adult masseters generally stain for either alkaline- or acid-stable mATPase activity, a substantial proportion of cells in developing animals exhibits the presence of both isozymes. EMG results indicate functional heterogeneity within the masseter of adult pigs. During chewing, when pig chow is replaced by cracked corn, EMG activity in the deep portion of the muscle either decreases or increases slightly. In the superficial portion, however, muscle amplitudes become dramatically higher for corn, surpassing levels generated for chewing the less obdurate chow. These results are consistent with a behavioral transition from neonatal suckling to sustained mastication of foods of more complex textures eaten by adult pigs. The relationship between these fiber type and EMG results for pig masseter corresponds to those pertaining to motor unit recruitment in the extensor muscles of locomotion. Implications of this work for the evolutionary morphology of mastication also are discussed.     

Sex differences in rabbit masseter motoneuron firing behavior

To evaluate whether sex differences in the proportions of fibers of different phenotypes in the masseter muscle might be the result of differences in the behavior of their motoneurons, we studied the firing patterns of masseter motoneurons in adult male and female rabbits. Activity in individual motoneurons was determined from high spatial resolution EMG recordings made during cortically evoked rhythmic activation of the masticatory muscles. Although some motoneurons could be said to fire according to slow-tonic or fast-phasic patterns, most did not. In both sexes a substantial range of median firing rates and median firing durations was found. In adult males, masseter motoneurons fired more rapidly than those recorded from adult females. No significant sex differences in motoneuron firing duration were found. These results are consistent with the hypothesis that androgen-induced differences in rabbit masseter muscle fiber phenotype are a reflection of differences in motoneuron firing rate. Whether this effect of androgen is directly upon the motoneurons or is the result of a response of muscle fibers to androgen remains to be investigated.     

Mandibular stiffness in humans: numerical predictions

The chin is a feature unique to humans. This study evaluates the effect of mandibular symphyseal design on biomechanical masticatory effectiveness as determined by structural stiffness and stress developed under flexural and torsional loading. A simple model of three symphyseal shapes (chin, flat symphysis and lingual buttress), was built to represent human, Neanderthal and higher primate symphyses and these were subjected to wishboning and torsional forces. Additionally, an anatomically detailed reconstruction was made of the CT scan of an actual human mandible, which was then also morphed into a chinless model. The results of a 3-D finite element analysis show firstly, that none of the three different symphyseal shapes is biomechanically more advantageous than the others for the given loading condition. Secondly, we show in a CT-derived model, that the presence of a chin does not confer significantly improved stiffness to torsional or flexural loading. These results indicate that the acquisition of a chin in modern humans is not related to the functional demands placed upon the mandible during mastication, but suggest that it may have developed in response to other biomechanical demands.     

Jaw morphology and function in living and fossil old world monkeys

This allometric investigation on a sample of 29 cercopithecine and 22 colobine taxa augments the data and implications of prior work on subfamilial variation in mandibular form and function in recent Cercopithecidae. To increase the size range encompassed by living cercopithecines and colobines, I included many of the larger-bodied fossil specimens. These analyses serve to fill a gap in our understanding of size-related changes in masticatory function and symphyseal morphology and curvature in extant and extinct Old World monkeys. Results of subfamilial scaling comparisons indicate that for a given jaw length, colobines possess significantly more robust corpora and symphyses than those of cercopithecines, especially at smaller sizes. Following from previous work, the most plausible explanation for why the subfamilies differ in relative corporeal and symphyseal dimensions is that colobine mandibles experience elevated loads and greater repetitive loading during mastication due, on average, to processing a diet of tough leaves and/or seeds. Although colobines have relatively larger symphyses, subfamilial analyses of symphyseal curvature demonstrate that they evince less symphyseal curvature vis-à-vis cercopithecines of a common size. Moreover, both subfamilies exhibit similar allometric changes in the degree of curvature, such that larger-bodied Old World monkeys have more curved symphyses than those of smaller taxa. Subfamilial scaling analyses also indicate that colobines possess a shorter M2 bite-point length relative to masseter lever-arm length, but not versus temporalis lever-arm length. Thus, as compared to cercopithecines, colobines can recruit less masseter-muscle force to produce similar bite forces during mastication. In both clades, M² bite-point length scales with positive allometry relative to masseter lever-arm length, such that larger species are less efficient at generating molar bite forces. This seems especially important due to the lack of subfamily difference in M² bite-point:temporalis lever-arm scaling (which is isometric across cercopithecids). A consideration of extinct cercopithecids indicates that many of the large-bodied papionins have more robust corpora, due perhaps to a diet which was of similar toughness to that of extant and extinct colobines. However, the biomechanical arrangements of the masseter and temporalis in all but one fossil cercopithecine and all of the fossil colobine specimens are much as predicted for a subfamilial member of its skull size. That most large-bodied papionins with tougher diets nonetheless maintain a less efficient jaw-muscle configuration may be due to stronger offsetting selection for increased relative canine size and gape.