Higher social tolerance is associated with more complex facial behavior in macaques.

The social complexity hypothesis for communicative complexity posits that animal societies with more complex social systems require more complex communication systems. We tested the social complexity hypothesis on three macaque species that vary in their degree of social tolerance and complexity. We coded facial behavior in >3000 social interactions across three social contexts (aggressive, submissive, affiliative) in 389 animals, using the Facial Action Coding System for macaques (MaqFACS). We quantified communicative complexity using three measures of uncertainty: entropy, specificity, and prediction error. We found that the relative entropy of facial behavior was higher for the more tolerant crested macaques as compared to the less tolerant Barbary and rhesus macaques across all social contexts, indicating that crested macaques more frequently use a higher diversity of facial behavior. The context specificity of facial behavior was higher in rhesus as compared to Barbary and crested macaques, demonstrating that Barbary and crested macaques used facial behavior more flexibly across different social contexts. Finally, a random forest classifier predicted social context from facial behavior with highest accuracy for rhesus and lowest for crested, indicating there is higher uncertainty and complexity in the facial behavior of crested macaques. Overall, our results support the social complexity hypothesis.

Tolerant macaque species are less impulsive and reactive.

Inhibitory control, the inhibition of impulsive behaviours, is believed to be key in navigating a complex social environment. Species characterised by higher social tolerance, living in more complex groups, with more diverse relationships, face higher uncertainty regarding the outcome of social interactions and, therefore, would benefit from employing more inhibitory strategies. To date, little is known about the selective forces that favour the evolution of inhibitory control. In this study, we compared inhibitory control skills in three closely related macaque species which differ in their social tolerance style. We tested 66 macaques from two institutions (Macaca mulatta, low tolerance; M. fascicularis, medium tolerance; and M. tonkeana, high tolerance) using a battery of validated inhibitory control touchscreen tasks. Higher social tolerance was associated with enhanced inhibitory control performances. More tolerant species were less impulsive and less distracted by pictures of unknown conspecifics. Interestingly, we did not find evidence that social tolerance degree was associated with performance in reversal learning. Overall, our results support the hypothesis that evolution has promoted the development of socio-cognitive skills to cope with the demands related to the complexity of the social environment.

Revisiting the baby schema by a geometric morphometric analysis of infant facial characteristics across great apes.

Infants across species are thought to exhibit specific facial features (termed the "baby schema", such as a relatively bigger forehead and eyes, and protruding cheeks), with an adaptive function to induce caretaking behaviour from adults. There is abundant empirical evidence for this in humans, but, surprisingly, the existence of a baby schema in non-human animals has not been scientifically demonstrated. We investigated which facial characteristics are shared across infants in five species of great apes: humans, chimpanzees, bonobos, mountain gorillas, and Bornean orangutans. We analysed eight adult and infant faces for each species (80 images in total) using geometric morphometric analysis and machine learning. We found two principal components characterizing infant faces consistently observed across species. These included (1) relatively bigger eyes located lower in the face, (2) a rounder and vertically shorter face shape, and (3) an inverted triangular face shape. While these features are shared, human infant faces are unique in that the second characteristic (round face shape) is more pronounced, whereas the third (inverted triangular face shape) is less pronounced than other species. We also found some infantile features only found in some species. We discuss future directions to investigate the baby schema using an evolutionary approach.

Personality Traits Predict Social Network Size in Older Adults.

Humans live in unusually large groups, where relationships are thought to be maintained through complex socio-communicative abilities. The size and quality of social networks are associated with health and well-being outcomes throughout life. However, how some individuals manage to form larger social networks is not well understood. If socio-communicative traits evolved to form and maintain relationships, personality traits should be associated with variation in network size. Here, using the English Longitudinal Study of Ageing (ELSA), we investigate the impact of extraversion, agreeableness, and verbal communication on network size (N = 5,202) and network size change over time (N = 1,511) in later life for kin and friend networks. Higher levels of extraversion and agreeableness were associated with greater social network sizes but did not predict network size change over 14 years. The findings are discussed considering the evolutionary hypothesis that communicative and affiliative traits may have evolved to support the maintenance of social networks.

Crested macaque facial movements are more intense and stereotyped in potentially risky social interactions.

Ambiguity in communicative signals may lead to misunderstandings and thus reduce the effectiveness of communication, especially in unpredictable interactions such as between closely matched rivals or those with a weak social bond. Therefore, signals used in these circumstances should be less ambiguous, more stereotyped and more intense. To test this prediction, we measured facial movements of crested macaques (Macaca nigra) during spontaneous social interaction, using the Facial Action Coding System for macaques (MaqFACS). We used linear mixed models to assess whether facial movement intensity and variability varied according to the interaction outcome, the individuals' dominance relationship and their social bond. Movements were least intense and most variable in affiliative contexts, and more intense in interactions between individuals who were closely matched in terms of dominance rating. We found no effect of social bond strength. Our findings provide evidence for a reduction in ambiguity of facial behaviour in risky social situations but do not demonstrate any mitigating effect of social relationship quality. The results indicate that the ability to modify communicative signals may play an important role in navigating complex primate social interactions. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Revisiting Darwin's comparisons between human and non-human primate facial signals.

Darwin and other pioneering scholars made comparisons between human facial signals and those of non-human primates, suggesting they share evolutionary history. We now have tools available (Facial Action Coding System: FACS) to make these comparisons anatomically based and standardised, as well as analytical methods to facilitate comparative studies. Here we review the evidence establishing a shared anatomical basis between the facial behaviour of human and non-human primate species, concluding which signals are likely related, and which are not. We then review the evidence for shared function and discuss the implications for understanding human communication. Where differences between humans and other species exist, we explore possible explanations and future directions for enquiry.

Validation of a battery of inhibitory control tasks reveals a multifaceted structure in non-human primates.

Inhibitory control, the ability to override an inappropriate prepotent response, is crucial in many aspects of everyday life. However, the various paradigms designed to measure inhibitory control often suffer from a lack of systematic validation and have yielded mixed results. Thus the nature of this ability remains unclear, is it a general construct or a family of distinct sub-components? Therefore, the aim of this study was first to demonstrate the content validity and the temporal repeatability of a battery of inhibitory control tasks. Then we wanted to assess the contextual consistency of performances between these tasks to better understand the structure of inhibitory control. We tested 21 rhesus macaques (Macaca mulatta, 12 males, nine females) in a battery of touchscreen tasks assessing three main components of inhibitory control: inhibition of a distraction (using a Distraction task), inhibition of an impulsive action (using a Go/No-go task) and inhibition of a cognitive set (using a Reversal learning task). All tasks were reliable and effective at measuring the inhibition of a prepotent response. However, while there was consistency of performance between the inhibition of a distraction and the inhibition of an action, representing a response-driven basic form of inhibition, this was not found for the inhibition of a cognitive set. We argue that the inhibition of a cognitive set is a more cognitively demanding form of inhibition. This study gives a new insight in the multifaceted structure of inhibitory control and highlights the importance of a systematic validation of cognitive tasks in animal cognition.

NetFACS: Using network science to understand facial communication systems.

Understanding facial signals in humans and other species is crucial for understanding the evolution, complexity, and function of the face as a communication tool. The Facial Action Coding System (FACS) enables researchers to measure facial movements accurately, but we currently lack tools to reliably analyse data and efficiently communicate results. Network analysis can provide a way to use the information encoded in FACS datasets: by treating individual AUs (the smallest units of facial movements) as nodes in a network and their co-occurrence as connections, we can analyse and visualise differences in the use of combinations of AUs in different conditions. Here, we present 'NetFACS', a statistical package that uses occurrence probabilities and resampling methods to answer questions about the use of AUs, AU combinations, and the facial communication system as a whole in humans and non-human animals. Using highly stereotyped facial signals as an example, we illustrate some of the current functionalities of NetFACS. We show that very few AUs are specific to certain stereotypical contexts; that AUs are not used independently from each other; that graph-level properties of stereotypical signals differ; and that clusters of AUs allow us to reconstruct facial signals, even when blind to the underlying conditions. The flexibility and widespread use of network analysis allows us to move away from studying facial signals as stereotyped expressions, and towards a dynamic and differentiated approach to facial communication.

Heterogeneity of performances in several inhibitory control tasks: male rhesus macaques are more easily distracted than females.

Inhibitory control, the ability to override a dominant response, is crucial in many aspects of everyday life. In animal studies, striking individual variations are often largely ignored and their causes rarely considered. Hence, our aims were to systematically investigate individual variability in inhibitory control, to replicate the most common causes of individual variation (age, sex and rank) and to determine if these factors had a consistent effect on three main components of inhibitory control (inhibition of a distraction, inhibition of an action, inhibition of a cognitive set). We tested 21 rhesus macaques (Macaca mulatta) in a battery of validated touchscreen tasks. We first found individual variations in all inhibitory control performances. We then demonstrated that males had poorer performances to inhibit a distraction and that middle-aged individuals exhibited poorer performance in the inhibition of a cognitive set. Hence, the factors of age and sex were not consistently associated with the main components of inhibitory control, suggesting a multi-faceted structure. The rank of the subjects did not influence any inhibitory control performances. This study adopts a novel approach for animal behaviour studies and gives new insight into the individual variability of inhibitory control which is crucial to understand its evolutionary underpinnings.

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.

Are there non-verbal signals of guilt?

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.

The social function of the feeling and expression of guilt.

Humans are uniquely cooperative and form crucial short- and long-term social bonds between individuals that ultimately shape human societies. The need for such intense cooperation may have provided a particularly powerful selection pressure on the emotional and communicative behaviours regulating cooperative processes, such as guilt. Guilt is a social, other-oriented moral emotion that promotes relationship repair and pro-sociality. For example, people can be more lenient towards wrongdoers who display guilt than towards those who do not. Here, we examined the social consequences of guilt in a novel experimental setting with pairs of friends differing in relationship quality. Pairs of participants took part in a cooperative game with a mutual goal. We then induced guilt in one of the participants and informed the other participant of their partner's wrongdoing. We examined the outcome using a dictator game to see how they split a joint reward. We found that guilty people were motivated to repair wrongdoing regardless of friendship. Observing guilt in others led to a punishment effect and a victim of wrongdoing punished close friends who appeared guilty more so than acquaintances. We suggest, therefore, that guilt has a stronger function between close friends as the costs of relationship breakdown are greater. Relationship context, therefore, is crucial to the functional relevance of moral emotions.

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.

Human attention affects facial expressions in domestic dogs.

Most mammalian species produce facial expressions. Historically, animal facial expressions have been considered inflexible and involuntary displays of emotional states rather than active attempts to communicate with others. In the current study, we aimed to test whether domestic dog facial expressions are subject to audience effects and/ or changes in response to an arousing stimulus (e.g. food) alone. We presented dogs with an experimental situation in which a human demonstrator was either attending to them or turned away, and varied whether she presented food or not. Dogs produced significantly more facial movements when the human was attentive than when she was not. The food, however, as a non-social but arousing stimulus, did not affect the dogs' behaviour. The current study is therefore evidence that dogs are sensitive to the human's attentional state when producing facial expressions, suggesting that facial expressions are not just inflexible and involuntary displays of emotional states, but rather potentially active attempts to communicate with others.

Stress behaviours buffer macaques from aggression.

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.

Comparing physical and social cognitive skills in macaque species with different degrees of social tolerance.

Contemporary evolutionary theories propose that living in groups drives the selection of enhanced cognitive skills to face competition and facilitate cooperation between individuals. Being able to coordinate both in space and time with others and make strategic decisions are essential skills for cooperating within groups. Social tolerance and an egalitarian social structure have been proposed as one specific driver of cooperation. Therefore, social tolerance is predicted to be associated with enhanced cognitive skills that underpin communication and coordination. Social tolerance should also be associated with enhanced inhibition, which is crucial for suppressing automatic responses and permitting delayed gratification in cooperative contexts. We tested the performance of four closely related non-human primate species (genus Macaca) characterized by different degrees of social tolerance on a large battery of cognitive tasks covering physical and social cognition, and on an inhibitory control task. All species performed at a comparable level on the physical cognition tasks but the more tolerant species outperformed the less tolerant species at a social cognition task relevant to cooperation and in the inhibitory control task. These findings support the hypothesis that social tolerance is associated with the evolution of sophisticated cognitive skills relevant for cooperative social living.

Is music enriching for group-housed captive chimpanzees (Pan troglodytes)?

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.

Exorcising Grice's ghost: an empirical approach to studying intentional communication in animals.

Language's intentional nature has been highlighted as a crucial feature distinguishing it from other communication systems. Specifically, language is often thought to depend on highly structured intentional action and mutual mindreading by a communicator and recipient. Whilst similar abilities in animals can shed light on the evolution of intentionality, they remain challenging to detect unambiguously. We revisit animal intentional communication and suggest that progress in identifying analogous capacities has been complicated by (i) the assumption that intentional (that is, voluntary) production of communicative acts requires mental-state attribution, and (ii) variation in approaches investigating communication across sensory modalities. To move forward, we argue that a framework fusing research across modalities and species is required. We structure intentional communication into a series of requirements, each of which can be operationalised, investigated empirically, and must be met for purposive, intentionally communicative acts to be demonstrated. Our unified approach helps elucidate the distribution of animal intentional communication and subsequently serves to clarify what is meant by attributions of intentional communication in animals and humans.