Evolution of facial muscle anatomy in dogs.

Domestication shaped wolves into dogs and transformed both their behavior and their anatomy. Here we show that, in only 33,000 y, domestication transformed the facial muscle anatomy of dogs specifically for facial communication with humans. Based on dissections of dog and wolf heads, we show that the levator anguli oculi medialis, a muscle responsible for raising the inner eyebrow intensely, is uniformly present in dogs but not in wolves. Behavioral data, collected from dogs and wolves, show that dogs produce the eyebrow movement significantly more often and with higher intensity than wolves do, with highest-intensity movements produced exclusively by dogs. Interestingly, this movement increases paedomorphism and resembles an expression that humans produce when sad, so its production in dogs may trigger a nurturing response in humans. We hypothesize that dogs with expressive eyebrows had a selection advantage and that "puppy dog eyes" are the result of selection based on humans' preferences.

Variation in Ontogenetic Facial Suture Fusion Patterns in Catarrhines.

Timing of craniofacial suture fusion is important for the determination of demographics and primate ontogeny. There has been much work concerning the timing of fusion of calvarial sutures over the last century, but little comprehensive work focusing on facial sutures. Here we assess the relationships of facial suture fusion across ontogeny among select catarrhines. Fusion timing patterns for 5 facial sutures were examined in 1,599 crania of Homo, Pan, Gorilla, Pongo, Hylobatidae, Papio, and Macaca. Calvarial volume (early ontogeny) and dental eruption (late ontogeny) were used as indicators of stage of development. General linear models, test for homogeneity of slopes, and ANOVA were used to determine differences in timing of fusion by taxon. For calvarial volume, taxonomic groups segregated by regression slopes, with models for Homo indicating sutural fusion throughout ontogeny, Pongo, Macaca, and Papio representing earlier and more complete suture fusion, and Pan, Gorilla, and Hylobatidae indicating very early facial suture fusion. Similar patterns are observed when dental eruption is used for developmental staging. Only Gorilla and Hylobatidae are observed to, generally, fuse all facial suture sites in adulthood. Finally, Homo appears to be unique in its delay and patency of sutures into late ontogeny. The taxonomic patterns of facial suture closure identified in this study likely reflect important evolutionary shifts in facial growth and development in catarrhines.

Morphological variants of silent bared-teeth displays have different social interaction outcomes in crested macaques (Macaca nigra).

OBJECTIVES: While it has been demonstrated that even subtle variation in human facial expressions can lead to significant changes in the meaning and function of expressions, relatively few studies have examined primate facial expressions using similarly objective and rigorous analysis. Construction of primate facial expression repertoires may, therefore, be oversimplified, with expressions often arbitrarily pooled and/or split into subjective pigeonholes. Our objective is to assess whether subtle variation in primate facial expressions is linked to variation in function, and hence to inform future attempts to quantify complexity of facial communication. MATERIALS AND METHODS: We used Macaque Facial Action Coding System, an anatomically based and hence more objective tool, to quantify "silent bared-teeth" (SBT) expressions produced by wild crested macaques engaging in spontaneous behavior, and utilized discriminant analysis and bootstrapping analysis to look for morphological differences between SBT produced in four different contexts, defined by the outcome of interactions: Affiliation, Copulation, Play, and Submission. RESULTS: We found that SBT produced in these contexts could be distinguished at significantly above-chance rates, indicating that the expressions produced in these four contexts differ morphologically. We identified the specific facial movements that were typically used in each context, and found that the variability and intensity of facial movements also varied between contexts. DISCUSSION: These results indicate that nonhuman primate facial expressions share the human characteristic of exhibiting meaningful subtle differences. Complexity of facial communication may not be accurately represented simply by building repertoires of distinct expressions, so further work should attempt to take this subtle variability into account.

A Novel Method for Assessing Enamel Thickness Distribution in the Anterior Dentition as a Signal for Gouging and Other Extractive Foraging Behaviors in Gummivorous Mammals.

Gummivory poses unique challenges to the dentition as gum acquisition may often require that the anterior teeth be adapted to retain a sharp edge and to resist loading because they sometimes must penetrate a highly obdurate substrate during gum extraction by means of gouging or scraping. It has been observed previously that the enamel on the labial surface of the teeth used for extraction is thicker relative to that on the lingual surface in taxa that extract gums, while enamel is more evenly distributed in the anterior teeth of taxa that do not regularly engage in extractive behaviors. This study presents a quantitative methodology for measuring the distribution of labial versus lingual enamel thickness among primate and marsupial taxa in the context of gummivory. Computed microtomography scans of 15 specimens representing 14 taxa were analyzed. Ten measurements were taken at 20% intervals starting from the base of the crown of the extractive tooth to the tip of the cutting edge across the lingual and labial enamel. A method for including worn or broken teeth is also presented. Mann-Whitney U tests, canonical variates analysis, and between-group principal components analysis were used to examine variation in enamel thickness across taxa. Our results suggest that the differential distribution of enamel thickness in the anterior dentition can serve as a signal for gouging behavior; this methodology distinguishes between gougers, scrapers, and nonextractive gummivores. Gouging taxa are characterized by significantly thicker labial enamel relative to the lingual enamel, particularly towards the crown tip. Examination of enamel thickness patterning in these taxa permits a better understanding of the adaptations for the extraction of gums in extant taxa and offers the potential to test hypotheses concerning the dietary adaptations of fossil taxa.

Social variables exert selective pressures in the evolution and form of primate mimetic musculature.

Mammals use their faces in social interactions more so than any other vertebrates. Primates are an extreme among most mammals in their complex, direct, lifelong social interactions and their frequent use of facial displays is a means of proximate visual communication with conspecifics. The available repertoire of facial displays is primarily controlled by mimetic musculature, the muscles that move the face. The form of these muscles is, in turn, limited by and influenced by phylogenetic inertia but here we use examples, both morphological and physiological, to illustrate the influence that social variables may exert on the evolution and form of mimetic musculature among primates. Ecomorphology is concerned with the adaptive responses of morphology to various ecological variables such as diet, foliage density, predation pressures, and time of day activity. We present evidence that social variables also exert selective pressures on morphology, specifically using mimetic muscles among primates as an example. Social variables include group size, dominance 'style', and mating systems. We present two case studies to illustrate the potential influence of social behavior on adaptive morphology of mimetic musculature in primates: (1) gross morphology of the mimetic muscles around the external ear in closely related species of macaque (Macaca mulatta and Macaca nigra) characterized by varying dominance styles and (2) comparative physiology of the orbicularis oris muscle among select ape species. This muscle is used in both facial displays/expressions and in vocalizations/human speech. We present qualitative observations of myosin fiber-type distribution in this muscle of siamang (Symphalangus syndactylus), chimpanzee (Pan troglodytes), and human to demonstrate the potential influence of visual and auditory communication on muscle physiology. In sum, ecomorphologists should be aware of social selective pressures as well as ecological ones, and that observed morphology might reflect a compromise between the demands of the physical and the social environments.

Exudativory in the Asian loris, Nycticebus: Evolutionary divergence in the toothcomb and M3.

OBJECTIVES: Slow lorises (Nycticebus spp.) are obligate exudativores that gouge tree bark. Dental adaptations for gouging within marmosets, the only other known primate obligate exudativore, are well-known but dental adaptations in Nycticebus are largely unidentified. In an effort to more completely understand potential dental adaptions within Nycticebus and the evolution of this dietary niche within Primates as an order, the present study examined dental morphometrics in the Asian lorises (Nycticebus and Loris). MATERIALS AND METHODS: We compared dental morphometrics between Nycticebus and the insectivorous slender lorises (Loris). Measurements from the toothcomb and select other teeth were taken from 92 specimens. Each variable was scaled by the geometric mean and resulting mean ratios were statistically compared between groups. A biomechanical shape variable was also calculated to estimate the ability of the toothcomb to resist bending that may be experienced during gouging. RESULTS: Toothcombs in Nycticebus were significantly (P < 0.05) more narrow, shorter, and thicker than those in Loris and had a higher calculated ability to withstand bending forces. Nycticebus also had reduced size in the last lower molar relative to Loris. CONCLUSIONS: The more robust, "squared off" toothcomb in Nycticebus matches behavioral observations that these primates gouge to access exudates. Results of the present study indicate that the toothcomb is the likely candidate for the dental tool used in gouging. The size reduction of the lower last molar in Nycticebus, a trait also found in a previous study in exudativorous galagos, may indicate that there is reduced selective pressure in a diet where little mastication would be needed to mechanically process exudates. These results may indicate that reduction in molar size could be a potential dental signature for exudativory, but further studies on a wider phylogenetic range of exudativorous primates would be necessary.

The vomeronasal organ of Lemur catta.

The vomeronasal organ (VNO), also known as the Jacobson's organ, is a bilateral chemosensory organ found at the base of the nasal cavity specialized for the detection of higher-molecular weight (non-volatile) chemostimuli. It has been linked to pheromone detection. The VNO has been well studied in nocturnal lemurs and lorises, but poorly studied in diurnal/cathemeral species despite the large repertoire of olfactory behaviors noted in species such as Lemur catta. Here, the VNO and associated structures were studied microanatomically in one adult female and one adult male L. catta. Traditional and immunohistochemical procedures demonstrate the VNO epithelium consists of multiple rows of sensory neurons. Immunoreactivity to Growth-associated protein 43 (GAP43) indicates the VNO is postnatally neurogenic. In volume, the VNO neuroepithelium scales similarly to palatal length compared to nocturnal strepsirrhines. Numerous taste buds present at the oral opening to the nasopalatine duct, with which the VNO communicates, provide an additional (or alternative) explanation for the flehmen behavior that has been observed in this species. The VNO of L. catta is shown to be microanatomically comparable to that of nocturnal strepsirrhines. Like nocturnal strepsirrhines, the VNO of L. catta may be functional in the reception of high-molecular weight secretions.

Dental caries in living and extinct strepsirrhines with insights into diet.

Dental caries is one of the most common diseases afflicting modern humans and occurs in both living and extinct non-human primates, as well as other mammalian species. Compared to other primates, less is known about the etiology or frequency of caries among the Strepsirrhini. Given the link between caries and diet, caries frequency may be informative about the dietary ecology of a given animal. Understanding rates of caries in wild populations is also critical to assessing dental health in captive populations. Here, we examine caries frequency in a sample of 36 extant strepsirrhine species (n = 316 individuals) using odontological collections of wild-, non-captive animals housed at the American Museum of Natural History by counting the number of specimens characterized by the disease. Additionally, in the context of studying caries lesions in strepsirrhines, case studies were also conducted to test if similar lesions were found in their fossil relatives. In particular, two fossil strepsirrhine species were analyzed: the earliest Late Eocene Karanisia clarki, and the subfossil lemur Megaladapis madagascariensis. Our results suggest that caries affects 13.92% of the extant individuals we examined. The frugivorous and folivorous taxa were characterized by the highest overall frequency of caries, whereas the insectivores, gummivores, and omnivores had much lower caries frequencies. Our results suggest that caries may be common among wild populations of strepsirrhines, and in fact is more prevalent than in many catarrhines and platyrrhines. These findings have important implications for understanding caries, diet, and health in living and fossil taxa.

Comparative histomorphology of intrinsic vibrissa musculature among primates: implications for the evolution of sensory ecology and "face touch".

Macrovibrissae are specialized tactile sensory hairs present in most mammalian orders, used in maxillary mechanoreception or "face touch." Some mammals have highly organized vibrissae and are able to "whisk" them. Movement of vibrissae is influenced by intrinsic vibrissa musculature, striated muscle bands that attach directly to the vibrissa capsule. It is unclear if primates have organized vibrissae or intrinsic vibrissa musculature and it is uncertain if they can move their vibrissae. The present study used histomorphological techniques to compare vibrissae among 19 primates and seven non-primate mammalian taxa. Upper lips of these mammals were sectioned and processed for histochemical analysis. While controlling for phylogenetic effects the following hypotheses were tested: 1) mammals with well-organized vibrissae possess intrinsic vibrissa musculature and 2) intrinsic vibrissa musculature is best developed in nocturnal, arboreal taxa. Our qualitative analyses show that only arboreal, nocturnal prosimians possess intrinsic musculature. Not all taxa that possessed organized vibrissae had intrinsic vibrissa musculature. Phylogenetic comparative analyses revealed a 70% probability that stem mammals, primates, and haplorhines possessed intrinsic vibrissa musculature and well-organized vibrissae. These two traits most likely coevolved according to a discrete phylogenetic analysis. These results indicate that nocturnal, arboreal primates have the potential to more actively use their vibrissae in spatial recognition and navigation tasks than diurnal, more terrestrial species, but there is a clear phylogenetic signal involved in the evolution of primate vibrissae and "face touch."

Mammalian facial muscles contain muscle spindles.

Muscle spindles are sensory receptors in skeletal muscle that provide information on muscle length and velocity of contraction. Previous studies noted that facial muscles lack muscle spindles, but recent reports indicate that the human platysma muscle and "buccal" muscles contain spindles. Mammalian facial muscles are active in social communication, vibrissa movement, and vocalizations, including human speech. Given these functions, we hypothesized that facial muscles contain muscle spindles, and we predicted that humans would have the greatest number, given the role our lips play in speech. We examined previously sectioned and stained (with H&E and trichrome stains) orbicularis oris (upper fibers) and zygomaticus (major) muscles across a broad phylogenetic range of mammalian species, spanning a wide distribution of body size and ecological niche, to assess the presence of muscle spindles. We also stained several sections with Sirius red to highlight the muscle spindle capsule. Our results indicate that mammalian facial muscles contain muscle spindles, supporting our hypothesis. Contrary to our prediction, though, humans (and other primates) had the lowest number of muscle spindles. We instead found that the carnivoran sample and the horse sample had the greatest number of spindles. Larger body size and nocturnality were also associated with a greater number of spindles. These results must be viewed with caution, though, as our sample size was small and there are critical mammalian taxa missing. Future work should use an expanded phylogenetic range of mammalian species to ascertain the role that phylogeny plays in muscle spindle presence and count.

Relaxin does not rescue coronal suture fusion in craniosynostotic rabbits.

OBJECTIVES: Craniosynostosis affects 1 in 2000 to 3000 live births and may result in craniofacial and neural growth disturbances. Histological data have shown that thick collagenous bundles are present in the sutural ligament, which may tether the osteogenic fronts, resulting in premature fusion. The hormone relaxin has been shown to disrupt collagen fiber organization, possibly preventing craniosynostosis by relaxing the sutural ligament and allowing osteogenic fronts to separate normally and stay patent. This study tested this hypothesis with a rabbit model of delayed-onset coronal suture synostosis. METHODS: A total of 18 New Zealand White rabbits with craniosynostosis were randomly assigned to one of three groups: sham control, protein control (BSA), relaxin treatment. After initial diagnosis, sham surgery, BSA, or relaxin was delivered to the fusing coronal suture in a slow-release (56-day) collagen vehicle. Longitudinal radiographs and body weights were collected at 10, 25, 42, and 84 days of age, and sutures were harvested for histology. RESULTS: Relaxin-treated animals had more disorganized intrasuture content than control groups. These specimens also appeared to have relatively wider sutures ectocranially. There were no significant differences in relaxin-treated animals for all craniofacial growth measures, or suture separation compared with controls. CONCLUSIONS: These data do not support our initial hypothesis that the use of relaxin may rescue sutures destined to undergo premature suture fusion. These findings suggest that collagen fiber arrangement may not be important for suture fusion. This protein therapy would not be clinically useful for craniosynostosis.

Finite element analysis of performance in the skulls of marmosets and tamarins.

Reliance on plant exudates is a relatively rare dietary specialization among mammals. One well-studied example of closely related exudate feeders is the New World marmosets and tamarins. Whereas marmosets actively gouge tree bark with their incisors to stimulate the flow of sap, tamarins are opportunistic exudate feeders that do not gouge bark. Several studies of the dentaries and jaw adductors indicate that marmosets exhibit specializations for increased gape at the expense of bite force. Few studies, however, have looked to the cranium of marmosets for evidence of functional specializations. Using 3D finite element models of the marmoset Callithrix jacchus and the tamarin Saguinus fuscicollis, we investigated the performance of the cranium under loading regimes that mimicked unilateral molar biting and bark-gouging. We investigated three measures of performance: the efficiency with which muscle force is transferred to bite force, the extent to which the models are stressed (a predictor of failure), and the work expended by muscles as they deform the skull (total strain energy). We found that during molar biting the two models exhibited similar levels of performance, though the Saguinus model had slightly higher mechanical efficiency, a slightly lower state of stress, and expended more energy on deformation. In contrast, under the bark-gouging load, Callithrix exhibited much higher mechanical efficiency than Saguinas, but did so at the expense of more work and higher levels of von Mises stress. This analysis illustrates that differences in the shapes of the skulls of Callithrix and Saguinus confer differences in performance. Whether these aspects of performance are targets of selection awaits broader comparative analyses.

Anatomical and ontogenetic influences on muscle density.

Physiological cross-sectional area (PCSA), an important biomechanical variable, is an estimate of a muscle's contractile force potential and is derived from dividing muscle mass by the product of a muscle's average fascicle length and a theoretical constant representing the density of mammalian skeletal muscle. This density constant is usually taken from experimental studies of small samples of several model taxa using tissues collected predominantly from the lower limbs of adult animals. The generalized application of this constant to broader analyses of mammalian myology assumes that muscle density (1) is consistent across anatomical regions and (2) is unaffected by the aging process. To investigate the validity of these assumptions, we studied muscles of rabbits (Oryctolagus cuniculus) in the largest sample heretofore investigated explicitly for these variables, and we did so from numerous anatomical regions and from three different age-cohorts. Differences in muscle density and histology as a consequence of age and anatomical region were evaluated using Tukey's HSD tests. Overall, we observed that older individuals tend to have denser muscles than younger individuals. Our findings also demonstrated significant differences in muscle density between anatomic regions within the older cohorts, though none in the youngest cohort. Approximately 50% of the variation in muscle density can be explained histologically by the average muscle fiber area and the average percent fiber area. That is, muscles with larger average fiber areas and a higher proportion of fiber area tend to be denser. Importantly, using the age and region dependent measurements of muscle density that we provide may increase the accuracy of PCSA estimations. Although we found statistically significant differences related to ontogeny and anatomical region, if density cannot be measured directly, the specific values presented herein should be used to improve accuracy. If a single muscle density constant that has been better validated than the ones presented in the previous literature is preferred, then 1.0558 and 1.0502 g/cm3 would be reasonable constants to use across all adult and juvenile muscles respectively.

Cranial synchondroses of primates at birth.

Cranial synchondroses are cartilaginous joints between basicranial bones or between basicranial bones and septal cartilage, and have been implicated as having a potential active role in determining craniofacial form. However, few studies have examined them histologically. Using histological and immunohistochemical methods, we examined all basicranial joints in serial sagittal sections of newborn heads from nine genera of primates (five anthropoids, four strepsirrhines). Each synchondrosis was examined for characteristics of active growth centers, including a zonal distribution of proliferating and hypertrophic chondrocytes, as well as corresponding changes in matrix characteristics (i.e., density and organization of Type II collagen). Results reveal three midline and three bilateral synchondroses possess attributes of active growth centers in all species (sphenooccipital, intrasphenoidal, presphenoseptal). One midline synchondrosis (ethmoseptal) and one bilateral synchondrosis (alibasisphenoidal synchondrosis [ABS]) are active growth centers in some but not all newborn primates. ABS is oriented more anteriorly in monkeys compared to lemurs and bushbabies. The sphenoethmoidal synchondrosis (SES) varies at birth: in monkeys, it is a suture-like joint (i.e., fibrous tissue between the two bones); however, in strepsirrhines, the jugum sphenoidale is ossified while the mesethmoid remains cartilaginous. No species possesses an SES that has the organization of a growth plate. Overall, our findings demonstrate that only four midline synchondroses have the potential to actively affect basicranial angularity and facial orientation during the perinatal timeframe, while the SES of anthropoids essentially transitions toward a "suture-like" function, permitting passive growth postnatally. Loss of cartilaginous continuity at SES and reorientation of ABS distinguish monkeys from strepsirrhines.

The facial expression musculature in primates and its evolutionary significance.

Facial expression is a mode of close-proximity non-vocal communication used by primates and is produced by mimetic/facial musculature. Arguably, primates make the most-intricate facial displays and have some of the most-complex facial musculature of all mammals. Most of the earlier ideas of primate mimetic musculature, involving its function in facial displays and its evolution, were essentially linear "scala natural" models of increasing complexity. More-recent work has challenged these ideas, suggesting that ecological factors and social systems have played a much larger role in explaining the diversity of structures than previously believed. The present review synthesizes the evidence from gross muscular, microanatomical, behavioral and neurobiological studies in order to provide a preliminary analysis of the factors responsible for the evolution of primate facial musculature with comparisons to general mammals. In addition, the unique structure, function and evolution of human mimetic musculature are discussed, along with the potential influential roles of human speech and eye gaze.

Effects of flutamide therapy on craniofacial growth and development in a model of craniosynostosis.

Research has implicated the faulty regulation of transforming growth factor beta signaling as one mechanism for premature calvaria suture fusion. Androgens have been shown to increase the expression and activity of the transforming growth factor beta, resulting in increased osteoblast proliferation and differentiation and possibly premature suture fusion. The present study was designed to test the hypothesis that flutamide, an androgen receptor-blocking agent, would "rescue" a coronal suture destined to fuse and improve craniofacial growth in a familial rabbit model of craniosynostosis. Thirty rabbits with delayed-onset, coronal suture synostosis were examined via longitudinal cephalometry. The rabbits were divided into 4 groups: (1) sham surgical controls (n = 10), (2) bovine serum albumin (500 ng) protein controls (n = 6), (3) flutamide diluent controls (n = 6), and (4) flutamide (15 mg dissolved in ethanol) experimental group (n = 8). At 10 days of age, radiopaque amalgam markers were implanted in all rabbits on either side of the coronal suture to monitor sutural growth. At 25 days of age, the bovine serum albumin, ethanol, and flutamide were combined with a slow-resorbing collagen vehicle and injected subperiosteally above the coronal suture into the respective groups. Although results revealed a slight but significant increase in coronal suture marker separation in flutamide-treated rabbits compared with controls at 42 days of age, few significant differences were noted for craniofacial growth and intracranial volume among groups. Results suggest that androgen receptor-blocking using flutamide may only provide a transient rescue to suture fusion in this model. Further research is needed to investigate the effects of hormones on suture development and maintenance.

Visualization and quantification of mimetic musculature via DiceCT.

The muscles of facial expression are of significant interest to studies of communicative behaviors. However, due to their small size and high integration with other facial tissues, the current literature is largely restricted to descriptions of the presence or absence of specific muscles. Using diffusible iodine-based contrast-enhanced computed tomography (DiceCT) to stain and digitally image the mimetic mask of Eulemur flavifrons (the blue-eyed black lemur), we demonstrate-for the first time-the ability to visualize these muscles in three-dimensional space and to measure their relative volumes. Comparing these data to earlier accounts of mimetic organization with the face of lemuroidea, we demonstrate several novel configurations within this taxon, particularly in the superior auriculolabialis and the posterior auricularis. We conclude that DiceCT facilitates the study these muscles in closer detail than has been previously possible, and offers significant potential for future studies of this anatomy.

Dental Signatures for Exudativory in Living Primates, with Comparisons to Other Gouging Mammals.

Exudativory, the consumption of gums, is an obligate or a facultative dietary niche for some primates and marsupials. Exudativory has been cited as a dietary niche that may have been present in early primates, so finding a dental signature for exudativory is highly desirable. The present study combines exudativorous lorisoids (galagos and lorises) into one sample to compare to closely related, non-exudativorous lorisoids to search for a consistent dental signature of exudativory. Linear measurements were taken from the toothcomb, P2 , M3 , upper canine, and P2 from skulls of 295 adult galagids and lorisids. Also, differential distribution of enamel on the anterior teeth was qualitatively investigated as a dental signature for gouging (a behavior that facilitates some exudativory) by micro-CT scanning one specimen each from two gougers, Nycticebus coucang and Callithrix jacchus, and two non-gougers, Perodicticus potto, and Saguinus fuscicollis. Non-primate gouging mammals, the vampire bat Desmodus rotundus and the sugar glider Petaurus breviceps, were compared to non-gouging relatives. Statistical analysis revealed that exudativorous galagos and lorises had significantly (P < 0.05) reduced M3 relative to non-exudativorous galagos and lorises. While the sample sizes for assessing enamel thickness were small, preliminary results show that gouging primates and non-primate mammals have reduced lingual enamel thickness on the anterior dentition compared to non-gouging relatives. We suggest that reduction of mastication, and, therefore, M3 dimensions are a likely dental signature for exudativory in Primates. While broader samples are needed to statistically confirm, differential distribution of enamel in the anterior dentition may also be a signature of exudativory. Anat Rec, 2019. © 2018 Wiley Periodicals, Inc. Anat Rec, 303:265-281, 2020. © 2018 American Association for Anatomy.

Vertical Clinging and Leaping Ahead: How Bamboo Has Shaped the Anatomy and Physiology of Hapalemur.

Hapalemur sps. and Prolemur simus (bamboo lemurs, collectively) stand out from the relatively homogeneous lemurids because they are bamboo feeders and vertical clingers and leapers. This unique diet presents equally unique challenges, like its verticality, toughness, and toxicity. The bamboo lemurs share the generalized anatomy of the other lemurids, but also display some well-documented skeletal adaptations, perhaps to overcome the problems presented by their specialization. Soft-tissue adaptations, however, remain largely unexplored. Explored here are possible soft-tissue adaptations in Hapalemur griseus. We compare H. griseus with other lemurids, Propithecus, Galago, Tarsier, and a tree shrew. Based on the available anatomical and physiological data, we hypothesize that Hapalemur and Prolemur species will have differences in hindlimb morphology when compared with other lemurids. We predict that H. griseus will have more hindlimb muscle mass and will amplify muscle mass differences with increased type II muscle fibers. Relative hindlimb muscle mass in H. griseus is less than other prosimians sampled, yet relative sural muscle mass is significantly heavier (P < 0.01) in H. griseus. Results show that the soleus muscle of H. griseus has a higher amount of type II (fast) fibers in plantarflexors. These findings indicate although H. griseus shares some generalized lemurid morphology, its diet of bamboo may have pushed this generalized lemurid to an anatomical extreme. We suspect additional bamboo-specific adaptations in their anatomy and physiology will be uncovered with further examination into the anatomy of the bamboo lemurs. Anat Rec, 2019. © 2019 Wiley Periodicals, Inc. Anat Rec, 303:295-307, 2020. © 2019 American Association for Anatomy.

Facial musculature in the rhesus macaque (Macaca mulatta): evolutionary and functional contexts with comparisons to chimpanzees and humans.

Facial expression is a common mode of visual communication in mammals but especially so in primates. Rhesus macaques (Macaca mulatta) have a well-documented facial expression repertoire that is controlled by the facial/mimetic musculature as in all mammals. However, little is known about the musculature itself and how it compares with those of other primates. Here we present a detailed description of the facial musculature in rhesus macaques in behavioral, evolutionary and comparative contexts. Formalin-fixed faces from six adult male specimens were dissected using a novel technique. The morphology, attachments, three-dimensional relationships and variability of muscles were noted and compared with chimpanzees (Pan troglodytes) and with humans. The results showed that there was a greater number of facial muscles in rhesus macaques than previously described (24 muscles), including variably present (and previously unmentioned) zygomaticus minor, levator labii superioris alaeque nasi, depressor septi, anterior auricularis, inferior auricularis and depressor supercilii muscles. The facial muscles of the rhesus macaque were very similar to those in chimpanzees and humans but M. mulatta did not possess a risorius muscle. These results support previous studies that describe a highly graded and intricate facial expression repertoire in rhesus macaques. Furthermore, these results indicate that phylogenetic position is not the primary factor governing the structure of primate facial musculature and that other factors such as social behavior are probably more important. The results from the present study may provide valuable input to both biomedical studies that use rhesus macaques as a model for human disease and disorder that includes assessment of facial movement and studies into the evolution of primate societies and communication.