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Darwin observed that form, and in his view, meaning, of facial behaviour (observable changes in the appearance of the face, often termed facial ‘expression’) is similar between a wide range of species and concluded that this must be due to a shared ancestral origin. Yet, as with all social behaviours, exactly how to define similarity and determine homology is debated. Facial behaviour is linked to specific facial muscle movements, so one important factor in determining homology is the anatomical basis of facial behaviours that appear similar in both appearance and social function. The Facial Action Coding System (FACS) was developed for the scientific measurement of human facial behaviour and is based on individual facial muscle movements (Ekman and Friesen, 1978). FACS has since been modified for use with various non-human primate species (chimpanzees, macaques, hylobatids, orangutans) and domestic species (dogs, cats, horses). These FACS can be used to trace continuity of form in facial behaviour across species and build a better understanding of the evolution of facial communication in mammals.

The studies were funded by a Leverhulme Trust Research Project Grant Cultural variation in the social function and expression of guilt awarded to the seventh and fourth authors (RPG-2016-206) and the Leverhulme Trust Research Project Grant Rethinking complexity in facial communication systems awarded to the sixth author (RPG-2018-334). Guilt is a complex emotion with a potentially important social function of stimulating cooperative behaviours towards and from others, but whether the feeling of guilt is associated with a recognisable pattern of nonverbal behaviour is unknown. We examined the production and perception of guilt in two different studies, with a total of 238 participants with various places of origin. Guilt was induced experimentally, eliciting patterns of movement that were associated with both the participants’ self-reported feelings of guilt and judges’ impressions of their guilt. Guilt was most closely associated with frowning and neck touching. While there were differences between self-reported guilt and perception of guilt the findings suggest that there are consistent patterns that could be considered a non-verbal signal of guilt in humans. Publisher PDF

Facial displays (or expressions) are a primary means of visual communication among conspecifics in many mammalian orders. Macaques are an ideal model among primates for investigating the co-evolution of facial musculature, facial displays, and social group size/behavior under the umbrella of "ecomorphology". While all macaque species share some social behaviors, dietary, and ecological parameters, they display a range of social dominance styles from despotic to tolerant. A previous study found a larger repertoire of facial displays in tolerant macaque species relative to despotic species. The present study was designed to further explore this finding by comparing the gross morphological features of mimetic muscles between the Sulawesi macaque (Macaca nigra), a tolerant species, and the rhesus macaque (M. mulatta), a despotic species. Five adult M. nigra heads were dissected and mimetic musculature was compared to those from M. mulatta. Results showed that there was general similarity in muscle presence/absence between the species as well as muscle form except for musculature around the external ear. M. mulatta had more musculature around the external ear than M. nigra. In addition, M. nigra lacked a zygomaticus minor while M. mulatta is reported to have one. These morphological differences match behavioral observations documenting a limited range of ear movements used by M. nigra during facial displays. Future studies focusing on a wider phylogenetic range of macaques with varying dominance styles may further elucidate the roles of phylogeny, ecology, and social variables in the evolution of mimetic muscles within Macaca Anat Rec, 299:1317-1324, 2016. © 2016 Wiley Periodicals, Inc.

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.

Primates (including humans) scratch when stressed. So far, such scratching has been seen as a by-product of physiological processes associated with stress, and attributed proximate, regulatory function. However, it is possible that others could use this relationship between scratching and stress as an indication of the animal’s stress state, and thus scratching could potentially have social function. As a test of this theory, we measured the production of, and social responses to scratching in a group of free-ranging rhesus macaques (Macaca mulatta). Firstly, we found that the likelihood of scratching was greater around periods of heightened social stress, such as being in proximity to high-ranking individuals, or non-friends. Secondly, when macaques scratched, subsequent interactions were less likely to be aggressive and more likely to be affiliative. Potential attackers may avoid attacking stressed individuals as stressed individuals could behave unpredictably or be weakened by their state of stress (rendering aggression risky and/or unnecessary). Observable stress behaviour could therefore have additional adaptive value by reducing the potential for escalated aggression, benefiting both senders and receivers by facilitating social cohesion. This basic ability to recognise stress in others could also be an important component in the evolution of social cognition such as empathy.

Many facilities that house captive primates play music for animal enrichment or for caregiver enjoyment. However, the impact on primates is unknown as previous studies have been inconclusive. We conducted three studies with zoo-housed chimpanzees (Pan troglodytes) and one with group-housed chimpanzees at the National Centre for Chimpanzee Care to investigate the effects of classical and pop/rock music on various variables that may be indicative of increased welfare. Study one compared the behaviour and use of space of 18 animals when silence, classical or pop/rock music was played into one of several indoor areas. Overall, chimpanzees did not actively avoid the area when music was playing but were more likely to exit the area when songs with higher beats per minute were broadcast. Chimpanzees showed significantly fewer active social behaviours when music, rather than silence, was playing. They also tended to be more active and engage in less abnormal behaviour during the music but there was no change to either self-grooming or aggression between music and silent conditions. The genre of music had no differential effects on the chimpanzees' use of space and behaviour. In the second study, continuous focal observations were carried out on three individuals with relatively high levels of abnormal behaviour. No differences in behaviour between music and silence periods were found in any of the individuals. The final two studies used devices that allowed chimpanzees to choose if they wanted to listen to music of various types or silence. Both studies showed that there were no persistent preferences for any type of music or silence. When taken together, our results do not suggest music is enriching for group-housed captive chimpanzees, but they also do not suggest that music has a negative effect on welfare.

Primate facial expressions (FEs) likely play an important role in primate society: through facial signals, individuals can potentially send and receive information and may benefit from coordinating their behavior accordingly. Many primates use a relaxed open mouth (ROM) facial display or “play face” (PF) during play behavior, where the mouth is open but teeth are covered. In addition to this conventional PF, however, Western Lowland gorillas (Gorilla gorilla gorilla) also use a full PF where the upper teeth are exposed. As the teeth are similarly exposed in the bared-teeth expression (which is a signal of appeasement, submission and/or affiliation), the full PF may be a blend of the PF and bared-teeth face, and have a different signal function to the PF alone. Focal animal sampling of captive Western Lowland gorillas (N = 10) showed that the full PF was more often observed in intense rather than gentle play, and intense play bouts that featured the full PF were longer than those that featured only the PF. Both expressions were associated with an increase in affinitive behavior between sender and receiver postplay, but only the full PF was associated with an increase higher than that of play alone. Overall, the findings suggest that the full PF has an additional role in coordinating and maintaining play, possibly though reducing uncertainty in the receiver and confirming that play is only play.

Insights into the character of social relations are rare but exciting glimpses when it comes to archaeological populations. This paper uses a multidisciplinary combination of archaeological and evolutionary biological approaches to assess the social value of the bared‐teeth motif (BTM) in pre‐Columbian iconography of the Greater Antilles. Bared teeth feature on discrete artifact categories within the material culture of many different groups in the Taino culture area after AD 1000. This BTM, usually part of facial anthropomorphic or zoomorphic decoration, is used for bodily adornments and items associated with healing and shamanic practices. It has generally been interpreted as representative of death, aggression, or the shamanic trance. However, the motif has never been examined in terms of its signal value as a positive facial expression. Studies of facial expression in human and nonhuman primates have shown that the bared‐teeth expression is used in social contexts as an unambiguous signal of nonaggres...

The rhesus macaque (Macaca mulatta) is the most utilized primate model in the biomedical and psychological sciences. Expressive behavior is of interest to scientists studying these animals, both as a direct variable (modeling neuropsychiatric disease, where expressivity is a primary deficit), as an indirect measure of health and welfare, and also in order to understand the evolution of communication. Here, intramuscular electrical stimulation of facial muscles was conducted in the rhesus macaque in order to document the relative contribution of each muscle to the range of facial movements and to compare the expressive function of homologous muscles in humans, chimpanzees and macaques. Despite published accounts that monkeys possess less differentiated and less complex facial musculature, the majority of muscles previously identified in humans and chimpanzees were stimulated successfully in the rhesus macaque and caused similar appearance changes. These observations suggest that the facial muscular apparatus of the monkey has extensive homology to the human face. The muscles of the human face, therefore, do not represent a significant evolutionary departure from those of a monkey species. Thus, facial expressions can be compared between humans and rhesus macaques at the level of the facial musculature, facilitating the systematic investigation of comparative facial communication.

The pioneering work of Duchenne (1862/1990) was replicated in humans using intramuscular electrical stimulation and extended to another species (Pan troglodytes: chimpanzees) to facilitate comparative facial expression research. Intramuscular electrical stimulation, in contrast to the original surface stimulation, offers the opportunity to activate individual muscles as opposed to groups of muscles. In humans, stimulation resulted in appearance changes in line with Facial Action Coding System (FACS) action units (AUs), and chimpanzee facial musculature displayed functional similarity to human facial musculature. The present results provide objective identification of the muscle substrate of human and chimpanzee facial expressions- data that will be useful in providing a common language to compare the units of human and chimpanzee facial expression.

Providing cognitive challenges to zoo-housed animals may provide enriching effects and subsequently enhance their welfare. Primates may benefit most from such challenges as they often face complex problems in their natural environment and can be observed to seek problem solving opportunities in captivity. However, the extent to which welfare benefits can be achieved through programmes developed primarily for cognitive research is unknown. We tested the impact of voluntary participation cognitive testing on the welfare of a socially housed group of crested macaques (Macaca nigra) at the Macaque Study Centre (Marwell Zoo). First, we compared the rate of self-directed and social behaviours on testing and non-testing days, and between conditions within testing days. Minimal differences in behaviour were found when comparing testing and non-testing days, suggesting that there was no negative impact on welfare as a result of cognitive testing. Lipsmacking behaviours were found to increase and aggressive interaction was found to decrease in the group as a result of testing. Second, social network analysis was used to assess the effect of testing on associations and interactions between individuals. The social networks showed that testing subjects increased their association with others during testing days. One interpretation of this finding could be that providing socially housed primates with an opportunity for individuals to separate from the group for short periods could help mimic natural patterns of sub-group formation and reunion in captivity. The findings suggest, therefore, that the welfare of captive primates can be improved through the use of cognitive testing in zoo environments.

How wolves were first domesticated is unknown. One hypothesis suggests that wolves underwent a process of selfdomestication by tolerating human presence and taking advantage of scavenging possibilities. The puppy-like physical andbehavioural traits seen in dogs are thought to have evolved later, as a byproduct of selection against aggression. Using speed of selection from rehoming shelters as a proxy for artificial selection, we tested whether paedomorphic features givedogs a selective advantage in their current environment. Dogs who exhibited facial expressions that enhance their neonatal appearance were preferentially selected by humans. Thus, early domestication of wolves may have occurred not only aswolf populations became tamer, but also as they exploited human preferences for paedomorphic characteristics. These findings, therefore, add to our understanding of early dog domestication as a complex co-evolutionary process.

Facial expression is a communication mode produced by facial (mimetic) musculature. Hylobatids (gibbons and siamangs) have a poorly documented facial display repertoire and little is known about their facial musculature. These lesser apes represent an opportunity to test hypotheses related to the evolution of primate facial musculature as they are the only hominoid with a monogamous social structure, and thus live in very small groups. Primate species living in large groups with numerous social relationships, such as chimpanzees and rhesus macaques, have been shown to have a complex facial display repertoire and a high number of discrete facial muscles. The present study was designed to examine the relative influence of social structure and phylogeny on facial musculature evolution by comparing facial musculature complexity among hylobatids, chimpanzees, and rhesus macaques. Four faces were dissected from four hylobatid species. Morphology, attachments, three-dimensional relationships, and variation among specimens were noted and compared to rhesus macaques and chimpanzees. Microanatomical characteristics of the orbicularis oris muscle were also compared. Facial muscles of hylobatids were generally gracile and less complex than both the rhesus macaque and chimpanzee. Microanatomically, the orbicularis oris muscle of hylobatids was relatively loosely packed with muscle fibers. These results indicate that environmental and social factors may have been important in determining morphology and complexity of facial musculature in the less social hylobatids and that they may not have experienced as strong selection pressure for mimetic muscle complexity as other, more social primates.

The orbicularis oris muscle plays a role in the production of primate facial expressions and vocalizations, nutrient intake, and in some non-human primates it is used as a prehensile, manipulative tool. As the chimpanzee (Pan troglodytes) is the closest living relative of humans, a comparison of the orbicularis oris muscle between these species may increase our understanding of the morphological specializations related to the differing functional demands of their lips and the factors responsible for their divergent evolution. To this end, this study compares the microanatomy of the mid-line upper fibers of the orbicularis oris muscle between chimpanzees and humans. A mid-line portion of the orbicularis oris muscle was harvested from the upper lips of three chimpanzee and five human cadavers. The sampled blocks included the area between the lateral borders of the nasal alar cartilages in both species. Each sample was processed for paraffin histology, sectioned and stained with a variety of protocols. Sections were examined for fiber direction and relative thickness of muscle layers. Ratios of cross-sectional connective tissue area vs. cross-sectional muscle tissue area, muscle fiber diameter and relative dermal thickness were calculated for each species. In both species, a clear pars marginalis layer was recognized, contrary to previous reports that only humans possess this layer. In chimpanzees, the relative fiber diameter and relative amount of muscle tissue (i.e. based on ratio of connective tissue area : muscle tissue area) were significantly (P < 0.05) greater than in humans. In contrast, measurements of relative dermal thickness showed that humans have a greater average dermal thickness of the upper lip than chimpanzees. Taken together, these results suggest that both human and chimpanzee orbicularis oris muscle upper fibers meet the specific functional demands associated with their divergent vocal and facial display repertoires, the development of human speech, and the use of the upper lip as a prehensile tool in chimpanzees.

Facial expression is heralded as a communication system common to all human populations, and thus is generally accepted as a biologically based, universal behavior. Happiness, sadness, fear, anger, surprise, and disgust are universally recognized and produced emotions, and communication of these states is deemed essential in order to navigate the social environment. It is puzzling, however, how individuals are capable of producing similar facial expressions when facial musculature is known to vary greatly among individuals. Here, the authors show that although some facial muscles are not present in all individuals, and often exhibit great asymmetry (larger or absent on one side), the facial muscles that are essential in order to produce the universal facial expressions exhibited 100% occurrence and showed minimal gross asymmetry in 18 cadavers. This explains how universal facial expression production is achieved, implies that facial muscles have been selected for essential nonverbal communicative function, and yet also accommodate individual variation.

The Chimpanzee Facial Action Coding System (ChimpFACS) is an objective, standardized observational tool for measuring facial movement in chimpanzees based on the well-known human Facial Action Coding System (FACS; P. Ekman & W. V. Friesen, 1978). This tool enables direct structural comparisons of facial expressions between humans and chimpanzees in terms of their common underlying musculature. Here the authors provide data on the first application of the ChimpFACS to validate existing categories of chimpanzee facial expressions using discriminant functions analyses. The ChimpFACS validated most existing expression categories (6 of 9) and, where the predicted group memberships were poor, the authors discuss potential problems with ChimpFACS and/or existing categorizations. The authors also report the prototypical movement configurations associated with these 6 expression categories. For all expressions, unique combinations of muscle movements were identified, and these are illustrated as peak intensity prototypical expression configurations. Finally, the authors suggest a potential homology between these prototypical chimpanzee expressions and human expressions based on structural similarities. These results contribute to our understanding of the evolution of emotional communication by suggesting several structural homologies between the facial expressions of chimpanzees and humans and facilitating future research.

Facial expressions are a critical mode of non-vocal communication for many mammals, particularly non-human primates. Although chimpanzees (Pan troglodytes) have an elaborate repertoire of facial signals, little is known about the facial expression (i.e. mimetic) musculature underlying these movements, especially when compared with some other catarrhines. Here we present a detailed description of the facial muscles of the chimpanzee, framed in comparative and phylogenetic contexts, through the dissection of preserved faces using a novel approach. The arrangement and appearance of muscles were noted and compared with previous studies of chimpanzees and with prosimians, cercopithecoids and humans. The results showed 23 mimetic muscles in P. troglodytes, including a thin sphincter colli muscle, reported previously only in adult prosimians, a bi-layered zygomaticus major muscle and a distinct risorius muscle. The presence of these muscles in such definition supports previous studies that describe an elaborate and highly graded facial communication system in this species that remains qualitatively different from that reported for other non-human primate species. In addition, there are minimal anatomical differences between chimpanzees and humans, contrary to conclusions from previous studies. These results amplify the importance of understanding facial musculature in primate taxa, which may hold great taxonomic value.

The social brain hypothesis proposes that large neocortex size in Homonoids evolved to cope with the increasing demands of complex group living and greater numbers of interindividual relationships. Group living requires that individuals communicate effectively about environmental and internal events. Recent data have highlighted the complexity of chimpanzee communication, including graded facial expressions and referential vocalizations. Among Hominoids, elaborate facial communication is accompanied by specializations in brain areas controlling facial movement. Finally, the evolution of empathy, or emotional awareness, might have a neural basis in specialized cells in the neocortex, that is, spindle cells that have been associated with self-conscious emotions, and mirror neurons that have recently been shown to activate in response to communicative facial gestures.

Although previous research reported that the visual feedback of a 'virtual arm' increased the control of a phantom arm, it did not consider that the repeated attempt to move the phantom may have contributed to the effect. Twenty-one lower limb amputees reported the response of their phantom leg during repeated attempts to move both legs in one of two conditions, a control condition in which the amputee only viewed the movements of their intact leg and an experimental condition in which the amputee additionally viewed the movements of a 'virtual' leg. It was found that viewing a virtual leg resulted in amputees reporting a significantly greater number of movements of their phantom leg than with attempted movement alone. The implications were discussed in terms of visuo-motor adaptation and theories of motor control.