Variation in Craniodental Pathologies Among Cercopithecoid Primates.

Pathologies of the skull and teeth are well documented for many human populations, but there are fewer studies of other primates. We contrast lesion prevalence and patterning among cercopithecoid primates and map variation onto socioecological variables. We compare craniodental lesions in six species: Nasalis larvatus (n = 54), Colobus polykomos (n = 64), Cercopithecus mitis (n = 65), Macaca fascicularis (n = 109), Theropithecus gelada (n = 13), and Papio anubis (n = 76). One of us (C.A.K.) evaluated each adult skull for multiple lesion types using standard criteria. We also tested for a relationship between lesion prevalence and cranial suture fusion (age proxy). We used nonparametric tests for sex and species differences as well as pathology co-occurrence in SPSS. Socioecological data come from previous studies. Sex differences in lesion prevalence were only detected in P. anubis. Within taxa, some lesion types co-occurred. In Macaca, the presence of caries was associated with several other lesion types. Pulp cavity exposure co-occurred with TMJ osteoarthritis in multiple taxa. Among taxa, male P. anubis had higher lesion prevalences, particularly related to the anterior dentition and facial trauma. Because we did not detect a relationship between suture fusion and lesion prevalence, we propose that craniodental lesions may also be influenced by socioecological variables such as group composition and ratio of fruit to leaves in the diet. Our findings suggest that pain from pulp cavity exposure and related dental infections may alter chewing biomechanics and contribute to onset of TMJ osteoarthritis in nonhuman primates, as seen in humans. Further, we suggest that higher lesion prevalence in male baboons is likely related to male-male competition. Skeletal lesion analysis provides useful insight into primate socioecology, particularly for rare or difficult-to-observe phenomena, and provides additional biological context for our own species.

Dental remains of Plio-Pleistocene Cercopithecidae (Mammalia: Primates) from Romania.

The superfamily Cercopithecoidea had a broad spatial distribution and occupied a wide variety of habitats across Europe from the Late Miocene until the Middle Pleistocene. Cercopithecines, such as macaques, showed more flexibility in habitat preferences, whereas colobines tended to be more sensitive to environmental differences. In Romania, only a few Pliocene and Pleistocene fossil sites have yielded primate remains. In this paper, we revise selected specimens previously listed in site reviews, and we describe several unpublished specimens from the Plio-Pleistocene fossil localities of Berești (Mammal Neogene [MN], MN14-MN15), Malușteni (MN14), Ciuperceni-2 (MN15b), and Betfia (MN18). For each, we provide detailed descriptions, comparisons to other relevant material, and updated taxonomic assignments. We also present an updated biochronology and provide a paleoenvironmental reconstruction based on the taxonomic composition of the faunal assemblages described from these primate localities. The colobine monkey Dolichopithecus ruscinensis, from Berești, Malușteni, and Ciuperceni-2, was present during the Early Pliocene in Romania. Mesopithecus monspessulanus is also known from Malușteni, as is Paradolichopithecus sp. The Early Pleistocene site Betfia yielded a molar germ (in crypt; Betfia-XIII) and a deciduous premolar (Betfia-IX), both belonging to a Macaca sylvanus subspecies. Macaca sylvanus ssp. occurrences from Betfia-XIII and Betfia-IX offer an important perspective for understanding the chronostratigraphic range and geographic distribution of this species during the Early Pleistocene. The paleoenvironmental descriptions from Ciuperceni-2 show that primates were distributed in a mosaic habitat, with open and forested areas and a warm Mediterranean climate. This differs from Malușteni, Berești, and Betfia, where a dry continental phase with an open landscape is inferred. Our review of paleoenvironmental conditions of Romanian primate localities provides a paleoecological framework for understanding the habitat preferences of extinct primates.

Ontogenetic biomechanics of tufted (Sapajus) and untufted (Cebus) capuchin mandibles.

OBJECTIVES: Cortical bone geometry is commonly used to investigate biomechanical properties of primate mandibles. However, the ontogeny of these properties is less understood. Here we investigate changes in cortical bone cross-sectional properties throughout capuchin ontogeny and compare captive versus wild, semi-provisioned groups. Tufted capuchins (Sapajus spp.) are known to consume relatively hard/tough foods, while untufted capuchins (Cebus spp.) exploit less mechanically challenging foods. Previous research indicates dietary differences are present early in development and adult Sapajus mandibles can resist higher bending/shear/torsional loads. MATERIALS AND METHODS: This study utilized microCT scans of 22 Cebus and 45 Sapajus from early infancy to adulthood from three sample populations: one captive Cebus, one captive Sapajus, and one semi-provisioned, free-ranging Sapajus. Mandibular cross-sectional properties were calculated at the symphysis, P3, and M1. If the tooth had not erupted, its position within the crypt was used. A series of one-way ANOVAs were performed to assess differences between and within the sample populations. RESULTS: Mandible robusticity increases across ontogeny for all three sample populations. Sapajus were better able to withstand bending and torsional loading even early in ontogeny, but no difference in shear resistance was found. Semi-provisioned, free-ranging Sapajus tend to show increased abilities to resist bending and torsional loading but not shear loading compared to captive Sapajus. DISCUSSION: This study helps advance our understanding of the primate masticatory system development and opens the door for further studies into adaptive plasticity in shaping the masticatory apparatus of capuchins and differences in captive versus free-ranging sample populations.

Tradeoffs between bite force and gape in Eulemur and Varecia.

In 1974, Sue Herring described the relationship between two important performance variables in the feeding system, bite force and gape. These variables are inversely related, such that, without specific muscular adaptations, most animals cannot produce high bite forces at large gapes for a given sized muscle. Despite the importance of these variables for feeding biomechanics and functional ecology, the paucity of in vivo bite force data in primates has led to bite forces largely being estimated through ex vivo methods. Here, we quantify and compare in vivo bite forces and gapes with output from simulated musculoskeletal models in two craniofacially distinct strepsirrhines: Eulemur, which has a shorter jaw and slower chewing cycle durations relative to jaw length and body mass compared to Varecia. Bite forces were collected across a range of linear gapes from 16 adult lemurs (suborder Strepsirrhini) at the Duke Lemur Center in Durham, North Carolina representing three species: Eulemur flavifrons (n = 6; 3F, 3M), Varecia variegata (n = 5; 3F, 2M), and Varecia rubra (n = 5; 5F). Maximum linear and angular gapes were significantly higher for Varecia compared to Eulemur (p = .01) but there were no significant differences in recorded maximum in vivo bite forces (p = .88). Simulated muscle models using architectural data for these taxa suggest this approach is an accurate method of estimating bite force-gape tradeoffs in addition to variables such as fiber length, fiber operating range, and gapes associated with maximum force. Our in vivo and modeling data suggest Varecia has reduced bite force capacities in favor of absolutely wider gapes compared to Eulemur in relation to their longer jaws. Importantly, our comparisons validate the simulated muscle approach for estimating bite force as a function of gape in extant and fossil primates.

Ontogenetic changes in jaw leverage and skull shape in tufted and untufted capuchins.

The ontogeny of feeding is characterized by shifting functional demands concurrent with changes in craniofacial anatomy; relationships between these factors will look different in primates with disparate feeding behaviors during development. This study examines the ontogeny of skull morphology and jaw leverage in tufted (Sapajus) and untufted (Cebus) capuchin monkeys. Unlike Cebus, Sapajus have a mechanically challenging diet and behavioral observations of juvenile Sapajus suggest these foods are exploited early in development. Landmarks were placed on three-dimensional surface models of an ontogenetic series of Sapajus and Cebus skulls (n = 53) and used to generate shape data and jaw-leverage estimates across the tooth row for three jaw-closing muscles (temporalis, masseter, medial pterygoid) as well as a weighted combined estimate. Using geometric morphometric methods, we found that skull shape diverges early and shape is significantly different between Sapajus and Cebus throughout ontogeny. Additionally, jaw leverage varies with age and position on the tooth row and is greater in Sapajus compared to Cebus when calculated at the permanent dentition. We used two-block partial least squares analyses to identify covariance between skull shape and each of our jaw muscle leverage estimates. Sapajus, but not Cebus, has significant covariance between all leverage estimates at the anterior dentition. Our findings show that Sapajus and Cebus exhibit distinct craniofacial morphologies early in ontogeny and strong covariance between leverage estimates and craniofacial shape in Sapajus. These results are consistent with prior behavioral and comparative work suggesting these differences are a function of selection for exploiting mechanically challenging foods in Sapajus, and further emphasize that these differences appear quite early in ontogeny. This research builds on prior work that has highlighted the importance of understanding ontogeny for interpreting adult morphology.

The impact of measurement technique and sampling on estimates of skeletal muscle fibre architecture.

Skeletal muscle fibre architecture provides important insights into performance of vertebrate locomotor and feeding behaviours. Chemical digestion and in situ sectioning of muscle bellies along their lengths to expose fibres, fibre orientation and intramuscular tendon, are two classical methods for estimating architectural variables such as fibre length (Lf) and physiological cross-sectional area (PCSA). It has recently been proposed that Lf estimates are systematically shorter and hence less accurate using in situ sectioning. Here we addressed this hypothesis by comparing Lf estimates between the two methods for the superficial masseter and temporalis muscles in a sample of strepsirrhine and platyrrhine primates. Means or single-specimen Lf estimates using chemical digestion were greater in 17/32 comparisons (53.13%), indicating the probability of achieving longer fibres using chemical digestion is no greater than chance in these taxonomic samples. We further explored the impact of sampling on scaling of Lf and PCSA in platyrrhines applying a bootstrapping approach. We found that sampling-both numbers of individuals within species and representation of species across the clade significantly influence scaling results of Lf and PCSA in platyrrhines. We show that intraspecific and clade sampling strategies can account for differences between previously published platyrrhine scaling studies. We suggest that differences in these two methodological approaches to assessing muscle architecture are relatively less consequential when estimating Lf and PCSA for comparative studies, whereas achieving more reliable estimates within species through larger samples and representation of the full clade space are important considerations in comparative studies of fibre architecture and scaling.

Skeletal age during hurricane impacts fluctuating asymmetry in Cayo Santiago rhesus macaques.

As natural disasters become more frequent due to climate change, understanding the biological impact of these ecological catastrophes on wild populations becomes increasingly pertinent. Fluctuating asymmetry (FA), or random deviations from bilateral symmetry, is reflective of developmental instability and has long been positively associated with increases in environmental stress. This study investigates craniofacial FA in a population of free-ranging rhesus macaques (Macaca mulatta) that has experienced multiple Category 3 hurricanes since the colony's inception on Cayo Santiago, including 275 individuals from ages 9 months to 31 years (F = 154; M = 121). Using geometric morphometrics to quantify FA and a linear mixed-effect model for analysis, we found that sex, age, and decade of birth did not influence the amount of FA in the individuals included in the study, but the developmental stage at which individuals experienced these catastrophic events greatly impacted the amount of FA exhibited (p = .001). Individuals that experienced these hurricanes during fetal life exhibited greater FA than any other post-natal developmental period. These results indicate that natural disasters can be associated with developmental disruption that results in long-term effects if occurring during the prenatal period, possibly due to increases in maternal stress-related hormones.

A medida que los desastres naturales se vuelven más frecuentes debido al cambio climático, entender el impacto biológico de estas catástrofes ecológicas en poblaciones silvestres va en aumento pertinente. La asimetría fluctuante (AF), o desviaciones aleatorias de simetría bilateral, es reflejo de inestabilidad durante el desarrollo y se ha asociado positivamente con incrementos en estrés ambiental durante mucho tiempo. Este estudio investiga AF craneofacial en una población de macacos rhesus (Macaca mulatta) en libertad que ha experimentado múltiples huracanes categoría 3 desde el inicio de la colonia en Cayo Santiago, e incluye 275 individuos de 9 meses a 31 años de edad (F = 154; M = 121). Usando morfometría geométrica para cuantificar AF y un modelo lineal de efectos mixtos para análisis, encontramos que el sexo, la edad y la década de nacimiento no influyeron en la cantidad de AF en los individuos incluidos en el estudio, pero la etapa de desarrollo en la que los individuos experimentaron estos eventos catastróficos impactó altamente la cantidad de AF exhibida (p = .001). Los individuos que experimentaron estos huracanes durante el período fetal exhibieron mayor AF que cualquier otro período de desarrollo posnatal. Estos resultados indican que los desastres naturales pueden asociarse con trastornos del desarrollo que tienen efectos a largo plazo si ocurren durante el período prenatal, posiblemente debido al aumento de hormonas maternas relacionadas con el estrés.

Ontogenetic changes in bite force and gape in tufted capuchins.

Bite force and gape are two important performance metrics of the feeding system, and these metrics are inversely related for a given muscle size because of fundamental constraints in sarcomere length-tension relationships. How these competing performance metrics change in developing primates is largely unknown. Here, we quantified in vivo bite forces and gapes across ontogeny and examined these data in relation to body mass and cranial measurements in captive tufted capuchins, Sapajus spp. Bite force and gape were also compared across geometric and mechanical properties of mechanically challenging foods to investigate relationships between bite force, gape and food accessibility (defined here as the ability to breach shelled nuts). Bite forces at a range of gapes and feeding behavioral data were collected from a cross-sectional ontogenetic series of 20 captive and semi-wild tufted capuchins at the Núcleo de Procriação de Macacos-Prego Research Center in Araçatuba, Brazil. These data were paired with body mass, photogrammetric measures of jaw length and facial width, and food geometric and material properties. Tufted capuchins with larger body masses had absolutely higher in vivo bite forces and gapes, and animals with wider faces had absolutely higher bite forces. Bite forces and gapes were significantly smaller in juveniles compared with subadults and adults. These are the first primate data to empirically demonstrate the gapes at which maximum active bite force is generated and to demonstrate relationships to food accessibility. These data advance our understanding of how primates meet the changing performance demands of the feeding system during development.

Temporomandibular joint shape in anthropoid primates varies widely and is patterned by size and phylogeny.

The temporomandibular joint is the direct interface between the mandible and the cranium and is critical for transmitting joint reaction forces and determining mandibular range of motion. As a consequence, understanding variation in the morphology of this joint and how it relates to other aspects of craniofacial form is important for better understanding masticatory function. Here, we present a detailed three-dimensional (3D) geometric morphometric analysis of the cranial component of this joint, the glenoid fossa, across a sample of 17 anthropoid primates, and we evaluate covariation between the glenoid and the cranium and mandible. We find high levels of intraspecific variation in glenoid shape that is likely linked to sexual dimorphism and joint remodeling, and we identify differences in mean glenoid shape across taxonomic groups and in relation to size. Analyses of covariation reveal strong relationships between glenoid shape and a variety of aspects of cranial and mandibular form. Our findings suggest that intraspecific variation in glenoid shape in primates could further be reflective of high levels of functional flexibility in the masticatory apparatus, as has also been suggested for primate jaw kinematics and muscle activation patterns. Conversely, interspecific differences likely reflect larger scale differences between species in body size and/or masticatory function. Results of the covariation analyses dovetail with those examining covariation in the cranium of canids and may be indicative of larger patterns across mammals.

Craniofacial fluctuating asymmetry in gorillas, chimpanzees, and macaques.

OBJECTIVES: Craniofacial fluctuating asymmetry (FA) refers to the random deviations from symmetry exhibited across the craniofacial complex and can be used as a measure of developmental instability for organisms with bilateral symmetry. This article addresses the lack of data on craniofacial FA in nonhuman primates by analyzing FA magnitude and variation in chimpanzees, gorillas, and macaques. We offer a preliminary investigation into how FA, as a proxy for developmental instability, varies within and among nonhuman primates. MATERIALS AND METHODS: We generated 3D surface models of 121 crania from Pan troglodytes troglodytes, Gorilla gorilla gorilla, and Macaca fascicularis fascicularis. Using geometric morphometric techniques, the magnitude of observed FA was calculated and compared for each individual, sex, and taxon, along with the variation of FA across cranial regions and for each bilateral landmark. RESULTS: Gorillas and macaques exhibited higher and more similar magnitudes of FA to each other than either taxon did to chimpanzees; variation in magnitude of FA followed this same trend. No significant differences were detected between sexes using pooled data across species, but sex did influence FA magnitude within taxa in gorillas. Further, variation in FA variance across cranial regions and by landmark was not distributed in any particular pattern. CONCLUSION: Possible environmentally induced causes for these patterns of FA magnitude include differences in growth rate and physiological stress experienced during life. Developmental stability may be greatest in chimpanzees in this sample. Additionally, these results point to appropriate landmarks for future FA analyses and may help suggest more urgent candidate taxa for conservation efforts.

Bolstering geometric morphometrics sample sizes with damaged and pathologic specimens: Is near enough good enough?

Obtaining coordinate data for geometric morphometric studies often involves the sampling of dry skeletal specimens from museum collections. But many specimens exhibit damage and/or pathologic conditions. Such specimens can be considered inadequate for the analyses of shape and are excluded from study. However, the influences that damaged specimens may have on the assessment of normal shape variation have only been explored in two-dimensional coordinate data and no studies have addressed the inclusion of pathological specimens to date. We collected three-dimensional coordinate data from the cranium and mandible of 100 crab-eating macaques (Macaca fascicularis). Tests typically employed to analyze shape variation were performed on five datasets that included specimens with varying degrees of damage/pathology. We hypothesized that the inclusion of these specimens into larger datasets would strengthen statistical support for dominant biological predictors of shape, such as sex and size. However, we also anticipated that the analysis of only the most questionable specimens may confound statistical outputs. We then analyzed a small sample of good quality specimens bolstered by specimens that would generally be excluded due to damage or pathologic morphology and compared the results with previous analyses. The inclusion of damaged/pathologic specimens in a larger dataset resulted in increased variation linked to allometry, sexual dimorphism, and covariation, supporting our initial hypothesis. We found that analyzing the most questionable specimens alone gave consistent results for the most dominant aspects of shape but could affect outputs for less influential principal components and predictors. The small dataset bolstered with damaged/pathologic specimens provided an adequate assessment of the major components of shape, but finer scale differences were also identified. We suggest that normal and repeatable variation contributed by specimens exhibiting damage and/or pathology emphasize the dominant components and shape predictors in larger datasets, however, the various unique conditions may be more influential for limited sample sizes. Furthermore, we find that exclusion of damaged/pathologic specimens can, in some cases, omit important demographic-specific shape variation of groups of individuals more likely to exhibit these conditions. These findings provide a strong case for inclusion of these specimens into studies that focus on the dominant aspects of intraspecific shape variation. However, they may present issues when testing hypotheses relating to more fine-scale aspects of morphology.

Internal architecture of the mandibular condyle of rabbits is related to dietary resistance during growth.

Although there is considerable evidence that bone responds to the loading environment in which it develops, few analyses have examined phenotypic plasticity or bone functional adaptation in the masticatory apparatus. Prior work suggests that masticatory morphology is sensitive to differences in food mechanical properties during development; however, the importance of the timing/duration of loading and variation in naturalistic diets is less clear. Here, we examined microstructural and macrostructural differences in the mandibular condyle in four groups of white rabbits (Oryctolagus cuniculus) raised for a year on diets that varied in mechanical properties and timing of the introduction of mechanically challenging foods, simulating seasonal variation in diet. We employed sliding semilandmarks to locate multiple volumes of interest deep to the mandibular condyle articular surface, and compared bone volume fraction, trabecular thickness and spacing, and condylar size/shape among experimental groups. The results reveal a shared pattern of bony architecture across the articular surface of all treatment groups, while also demonstrating significant among-group differences. Rabbits raised on mechanically challenging diets have significantly increased bone volume fraction relative to controls fed a less challenging diet. The post-weaning timing of the introduction of mechanically challenging foods also influences architectural properties, suggesting that bone plasticity can extend well into adulthood and that bony responses to changes in loading may be rapid. These findings demonstrate that bony architecture of the mandibular condyle in rabbits responds to variation in mechanical loading during an organism's lifetime and has the potential to track dietary variation within and among species.

Individual variation of the masticatory system dominates 3D skull shape in the herbivory-adapted marsupial wombats.

BACKGROUND: Within-species skull shape variation of marsupial mammals is widely considered low and strongly size-dependent (allometric), possibly due to developmental constraints arising from the altricial birth of marsupials. However, species whose skulls are impacted by strong muscular stresses - particularly those produced through mastication of tough food items - may not display such intrinsic patterns very clearly because of the known plastic response of bone to muscle activity of the individual. In such cases, allometry may not dominate within-species shape variation, even if it is a driver of evolutionary shape divergence; ordination of shape in a geometric morphometric context through principal component analysis (PCA) should reveal main variation in areas under masticatory stress (incisor region/zygomatic arches/mandibular ramus); but this main variation should emerge from high individual variability and thus have low eigenvalues. RESULTS: We assessed the evidence for high individual variation through 3D geometric morphometric shape analysis of crania and mandibles of three species of grazing-specialized wombats, whose diet of tough grasses puts considerable strain on their masticatory system. As expected, we found little allometry and low Principal Component 1 (PC1) eigenvalues within crania and mandibles of all three species. Also as expected, the main variation was in the muzzle, zygomatic arches, and masticatory muscle attachments of the mandibular ramus. We then implemented a new test to ask if the landmark variation reflected on PC1 was reflected in individuals with opposite PC1 scores and with opposite shapes in Procrustes space. This showed that correspondence between individual and ordinated shape variation was limited, indicating high levels of individual variability in the masticatory apparatus. DISCUSSION: Our results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern. Rather, they support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials (and possibly other mammals) with high masticatory stresses, making it difficult to understand the degree to which intrinsic constraints act on shape variation at the within-species level. We conclude that studies that link micro- and macroevolutionary patterns of shape variation might benefit from a focus on species with low-impact mastication, such as carnivorous or frugivorous species.

Sex and Height Influence Neck Posture When Using Electronic Handheld Devices.

With increased tablet ownership in the United States comes increased levels of neck flexion compared to desktop or laptop computer use, and these neck postures have been linked to increases in neck pain. Importantly, tablet viewing postures can be achieved in multiple ways and could be determined by the morphology of the individual and/or other extraneous factors. In this study, we aim to preliminarily evaluate how neck postures vary during tablet use among individuals and link this variation to other factors such as sex, height, weight, presence/absence of temporomandibular joint disorder (TMD), and morphology of the head and neck. We analyzed two-dimensional landmarks placed on lateral-view radiographs of 22 participants (10 female and 12 male) seated in neutral, upright, fully flexed, semi-reclined, and reclined postures. We utilize geometric morphometric techniques, which are advantageous for evaluating shape variation and have not been extensively applied to biomechanical analyses. We found skeletal morphology to be significantly related to sex and height in all but the neutral posture (P < 0.05), and weight was marginally significantly related to shape in the semi-reclined posture (P = 0.047). Morphologically, male participants exhibited more flexion at the articulatio atlantooccipitalis than females, and females showed greater mandibular protrusion than males, although this result is likely related to height. No relationship was found between posture and TMD. This research establishes a framework for future work that uses geometric morphometric analyses to evaluate how neck postures vary in relation to TMD. Clin. Anat. 32:1061-1071, 2019. © 2019 Wiley Periodicals, Inc.

The influence of masseter and temporalis sarcomere length operating ranges as determined by laser diffraction on architectural estimates of muscle force and excursion in macaques (Macaca fascicularis and Macaca mulatta).

OBJECTIVE: Determine sarcomere length (Ls) operating ranges of the superficial masseter and temporalis in vitro in a macaque model and examine the impact of position-dependent variation on Ls and architectural estimates of muscle function (i.e., fiber length, PCSA) before and after Ls-normalization. DESIGN: Heads of adult Macaca fascicularis (n = 4) and M. mulatta (n = 3) were bisected postmortem. One side of the jaw was fixed in occlusion, the other in maximum gape. Ls was measured bilaterally using laser diffraction and these measurements were used to estimate sarcomere-length operating ranges. Differences in fiber length and PCSA between sides were tested for significance prior to and following Ls-normalization. RESULTS: Sarcomere-length operating ranges were widest for the anterior superficial masseter and narrowest for the posterior temporalis. Compared with other mammals, macaque operating ranges were wider and shifted to the right of the descending limb of a representative length-tension curve. Fibers were significantly stretched by as much as 100%, and PCSAs reduced by as much as 43%, on the maximally gaped compared with occluded sides. Ls-normalization substantially reduced position-dependent variance. CONCLUSIONS: The superficial masseter ranges between 87-143% and the temporalis between 88-130% of optimal Ls from maximum gape to occlusion, indicating maximum relative Ls for these macaque muscles exceeds the upper end range previously reported for the jaw muscles of smaller mammals. The wider macaque operating ranges may be functionally linked to the propensity for facially prognathic primates to engage in agonistic canine display behaviors that require jaw-muscle stretch to facilitate production of wide jaw gapes.

Mandibular ramus shape variation and ontogeny in Homo sapiens and Homo neanderthalensis.

As the interface between the mandible and cranium, the mandibular ramus is functionally significant and its morphology has been suggested to be informative for taxonomic and phylogenetic analyses. In primates, and particularly in great apes and humans, ramus morphology is highly variable, especially in the shape of the coronoid process and the relationship of the ramus to the alveolar margin. Here we compare ramus shape variation through ontogeny in Homo neanderthalensis to that of modern and fossil Homo sapiens using geometric morphometric analyses of two-dimensional semilandmarks and univariate measurements of ramus angulation and relative coronoid and condyle height. Results suggest that ramus, especially coronoid, morphology varies within and among subadult and adult modern human populations, with the Alaskan Inuit being particularly distinct. We also identify significant differences in overall anterosuperior ramus and coronoid shapes between H. sapiens and H. neanderthalensis, both in adults and throughout ontogeny. These shape differences are subtle, however, and we therefore suggest caution when using ramus morphology to diagnose group membership for individual specimens of these taxa. Furthermore, we argue that these morphologies are unlikely to be representative of differences in masticatory biomechanics and/or paramasticatory behaviors between Neanderthals and modern humans, as has been suggested by previous authors. Assessments of ontogenetic patterns of shape change reveal that the typical Neanderthal ramus morphology is established early in ontogeny, and there is little evidence for divergent postnatal ontogenetic allometric trajectories between Neanderthals and modern humans as a whole. This analysis informs our understanding of intraspecific patterns of mandibular shape variation and ontogeny in H. sapiens and can shed further light on overall developmental and life history differences between H. sapiens and H. neanderthalensis.

Jaw-Muscle Fiber Architecture and Leverage in the Hard-Object Feeding Sooty Mangabey are not Structured to Facilitate Relatively Large Bite Forces Compared to Other Papionins.

Numerous studies have sought to link craniofacial morphology with behavioral ecology in primates. Extant hard-object feeders have been of particular interest because of their potential to inform our understanding about the diets of early fossil hominins. Sooty mangabeys (Cercocebus atys) are hard-object feeders that frequently generate what have been described as audibly powerful bites at wide jaw gapes to process materially stiff and hard seeds. We address the hypothesis that sooty mangabeys have features of the masticatory apparatus that facilitate this feeding behavior by comparing fiber architecture and leverage of the masseter and temporalis muscles between sooty mangabeys and three papionin primates that do not specialize on hard objects. Contrary to predictions, sooty mangabeys do not have relatively larger muscle physiologic cross-sectional areas or weights compared to other papionins, nor do they consistently display improved leverage. In this regard, sooty mangabeys differ in their morphology from other hard-object feeders such as tufted capuchins. However, males of all four papionin species converge on a shared pattern of relatively longer anterior superficial masseter fibers compared with female conspecifics, suggesting that males are likely prioritizing muscle stretch to improve gape performance as part of a behavioral repertoire that includes agonistic social interactions and intense male-male competition. These findings strengthen support for the hypothesis that gape display behaviors can exert a strong selective influence throughout the musculoskeletal masticatory apparatus. Results also raise questions about the morphological suitability of extant cercopithecines as models for interpreting feeding behavior and diet in fossil hominins with limited jaw gape capacity. Anat Rec, 301:325-342, 2018. © 2018 Wiley Periodicals, Inc.

Functional correlates of the position of the axis of rotation of the mandible during chewing in non-human primates.

The location of the axis of rotation (AoR) of the mandible was quantified using the helical axis (HA) in eight individuals from three species of non-human primates: Papio anubis, Cebus apella, and Macaca mulatta. These data were used to test three hypotheses regarding the functional significance of anteroposterior condylar translation - an AoR located inferior to the temporomandibular joint (TMJ) - during chewing: minimizing impingement of the gonial region on cervical soft tissue structures during jaw opening; avoiding stretching of the inferior alveolar neurovascular bundle (IANB); and increasing jaw-elevator muscle torques. The results reveal that the HA is located near the occlusal plane in Papio and Cebus, but closer to the condyle in Macaca; is located anteroinferior to the TMJ during both opening and closing in Papio, as well as during opening in Macaca and Cebus; and varies in its location during closing in Macaca and Cebus. The impingement hypothesis is not supported by interspecific variation in HA location: species with larger gonial angles like Cebus do not have more inferiorly located HAs than species with more obtuse mandibular angles like Papio. However, intraspecific variation provides some support for the impingement hypothesis. The HA seldom passes near or through the lingula, falsifying the hypothesis that its location is determined by the sphenomandibular ligament, and the magnitudes of strain associated with a HA at the TMJ would not be large enough to cause problematic stretching of the IANB. HA location does affect muscle moment arms about the TMJ, with implications for the torque generation capability of the jaw-elevator muscles. In Cebus, a HA farther away from the TMJ is associated with larger jaw-elevator muscle moment arms about the joint than if it were at the TMJ. The effects of HA location on muscle strain and muscle moment arms are largest at large gapes and smallest at low gapes, suggesting that if HA location is of functional significance for primate feeding system performance, it is more likely to be in relation to large gape feeding behaviors than chewing. Its presence in humans is most parsimoniously interpreted as a primitive retention from non-human primate ancestors and explanations for the presence of anteroposterior condylar translation in humans need not invoke either the uniqueness of human speech or upright posture.

Revisiting size and scaling in the anthropoid temporomandibular joint.

Masticatory morphology in primates is likely under strong selective pressure to maximize feeding efficiency while simultaneously minimizing the occurrence of injury or pathology. As a result, masticatory shape, including aspects of temporomandibular joint (TMJ) morphology, varies widely across primates in relation to feeding behavior and body size. This study examines patterns of allometry in the TMJ of anthropoid primates, with the specific goal of evaluating how allometric patterns may reflect variation in loading and/or range of motion at this joint. Phylogenetic reduced major axis regressions were employed to examine how specific aspects of TMJ morphology scale in relation to body mass and mandible length. Patterns of shape variation across the entire masticatory apparatus were examined by utilizing geometric morphometric techniques. Results reveal that most aspects of TMJ shape scale with either isometry or positive allometry relative to body mass and/or mandible length, though several departures from these patterns were observed. In particular, male cercopithecoids tend to show distinct scaling patterns in TMJ height above the occlusal plane and condylar area, likely reflecting known trade-offs between increased range of motion and force production in this clade, as has been linked to selection for increased male canine size. The geometric morphometric analyses indicate that craniofacial and masticatory shape are strongly allometric, but that glenoid shape variation is less consistently allometric. Notably, different patterns of allometric shape variation were observed in platyrrhines, cercopithecoids, and hominoids, perhaps related to different, and potentially competing, selective pressures in each of these clades.

Error in geometric morphometric data collection: Combining data from multiple sources.

OBJECTIVES: This study compares two- and three-dimensional morphometric data to determine the extent to which intra- and interobserver and intermethod error influence the outcomes of statistical analyses. MATERIALS AND METHODS: Data were collected five times for each method and observer on 14 anthropoid crania using calipers, a MicroScribe, and 3D models created from NextEngine and microCT scans. ANOVA models were used to examine variance in the linear data at the level of genus, species, specimen, observer, method, and trial. Three-dimensional data were analyzed using geometric morphometric methods; principal components analysis was employed to examine how trials of all specimens were distributed in morphospace and Procrustes distances among trials were calculated and used to generate UPGMA trees to explore whether all trials of the same individual grouped together regardless of observer or method. RESULTS: Most variance in the linear data was at the genus level, with greater variance at the observer than method levels. In the 3D data, interobserver and intermethod error were similar to intraspecific distances among Callicebus cupreus individuals, with interobserver error being higher than intermethod error. Generally, taxa separate well in morphospace, with different trials of the same specimen typically grouping together. However, trials of individuals in the same species overlapped substantially with one another. CONCLUSION: Researchers should be cautious when compiling data from multiple methods and/or observers, especially if analyses are focused on intraspecific variation or closely related species, as in these cases, patterns among individuals may be obscured by interobserver and intermethod error. Conducting interobserver and intermethod reliability assessments prior to the collection of data is recommended.