Lorenz's classic 'baby schema': a useful biological concept?

Konrad Lorenz introduced the concept of a 'baby schema', suggesting that infants have specific physical features, such as a relatively large head, large eyes and protruding cheeks, which function as an innate releaser to promote caretaking motivation from perceivers. Over the years, a large body of research has been conducted on the baby schema. However, there are two critical problems underpinning the current literature. First, the term 'baby schema' lacks consistency among researchers. Some researchers use the term baby schema to refer to infant stimuli (often faces) in comparison with adults (categorical usage), while others use the term to refer to the extent that features contribute to cuteness perception (spectrum usage). Second, cross-species continuity of the 'baby schema' has been assumed despite few empirical demonstrations. The evolutionary and comparative relevance of the concept is, therefore, debatable, and we cannot exclude the possibility that extreme sensitivity to the baby schema is a uniquely human trait. This article critically reviews the state of the existing literature and evaluates the significance of the baby schema from an evolutionary perspective.

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.

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.

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.

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.

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.

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.

Macaques can predict social outcomes from facial expressions.

There is widespread acceptance that facial expressions are useful in social interactions, but empirical demonstration of their adaptive function has remained elusive. Here, we investigated whether macaques can use the facial expressions of others to predict the future outcomes of social interaction. Crested macaques (Macaca nigra) were shown an approach between two unknown individuals on a touchscreen and were required to choose between one of two potential social outcomes. The facial expressions of the actors were manipulated in the last frame of the video. One subject reached the experimental stage and accurately predicted different social outcomes depending on which facial expressions the actors displayed. The bared-teeth display (homologue of the human smile) was most strongly associated with predicted friendly outcomes. Contrary to our predictions, screams and threat faces were not associated more with conflict outcomes. Overall, therefore, the presence of any facial expression (compared to neutral) caused the subject to choose friendly outcomes more than negative outcomes. Facial expression in general, therefore, indicated a reduced likelihood of social conflict. The findings dispute traditional theories that view expressions only as indicators of present emotion and instead suggest that expressions form part of complex social interactions where individuals think beyond the present.

Facial expression recognition in crested macaques (Macaca nigra).

Facial expressions are a main communication channel used by many different species of primate. Despite this, we know relatively little about how primates discriminate between different facial expressions, and most of what we do know comes from a restricted number of well-studied species. In this study, three crested macaques (Macaca nigra) took part in matching-to-sample tasks where they had to discriminate different facial expressions. In a first experiment, the macaques had to match a photograph of a facial expression to another exemplar of the same expression produced by a different individual, against examples of one of three other types of expressions and neutral faces. In a second experiment, they had to match a dynamic video recording of a facial expression to a still photograph of another exemplar of the same facial expression produced by another individual, also against one of four other expressions. The macaques performed above chance in both tasks, identifying expressions as belonging to the same category regardless of individual identity. Using matrix correlations and multidimensional scaling, we analysed the pattern of errors to see whether overall similarity between facial expressions and/or specific morphological features caused the macaques to confuse facial expressions. Overall similarity, measured with the macaque facial action coding system (maqFACS), did not correlate with performances. Instead, functional similarities between facial expressions could be responsible for the observed pattern of error. These results expand previous findings to a novel primate species and highlight the potential of using video stimuli to investigate the perception and categorisation of visual signals in primates.

Being facially expressive is socially advantageous.

Individuals vary in how they move their faces in everyday social interactions. In a first large-scale study, we measured variation in dynamic facial behaviour during social interaction and examined dyadic outcomes and impression formation. In Study 1, we recorded semi-structured video calls with 52 participants interacting with a confederate across various everyday contexts. Video clips were rated by 176 independent participants. In Study 2, we examined video calls of 1315 participants engaging in unstructured video-call interactions. Facial expressivity indices were extracted using automated Facial Action Coding Scheme analysis and measures of personality and partner impressions were obtained by self-report. Facial expressivity varied considerably across participants, but little across contexts, social partners or time. In Study 1, more facially expressive participants were more well-liked, agreeable, and successful at negotiating (if also more agreeable). Participants who were more facially competent, readable, and perceived as readable were also more well-liked. In Study 2, we replicated the findings that facial expressivity was associated with agreeableness and liking by their social partner, and additionally found it to be associated with extraversion and neuroticism. Findings suggest that facial behaviour is a stable individual difference that proffers social advantages, pointing towards an affiliative, adaptive function.

Multicomponent and multimodal lipsmacking in crested macaques (Macaca nigra).

Primates' communicative signals are often dynamic and composed of multiple components, sometimes belonging to different sensory modalities. Such multicomponent signals are of crucial importance in the study of communication: the addition of extra features to a signal has the potential to modulate or change the meaning and message of the specific signal. Traditionally, however, components of compound signals are studied in isolation from each other, or communicative displays are studied as static and invariant wholes. Both approaches may not allow us to assess the full function of the signals. In crested macaques (Macaca nigra), the lipsmack (a display mainly used in affiliative interactions) can be produced alone or combined with other visual and acoustic communicative features. We investigated whether the composition of the lipsmack influenced the outcome of social interaction while controlling for relationship quality. Our results show that lipsmacks composed of both visual and vocal components (i.e. multimodal signals) increased the probability of affiliative contact, and therefore have enhanced signal value. The total number of visual components involved in the display had no effect but some visual components seemed more influential than others. By analyzing lipsmacking behavior as a composite, dynamic display, we were able to reveal a level of complexity that is not apparent when looking at each component separately. The results highlight the importance of a more integrative, multimodal approach to the study of primate communication.

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.

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.

Social bonds affect anti-predator behaviour in a tolerant species of macaque, Macaca nigra.

Enduring positive social bonds between individuals are crucial for humans' health and well being. Similar bonds can be found in a wide range of taxa, revealing the evolutionary origins of humans' social bonds. Evidence suggests that these strong social bonds can function to buffer the negative effects of living in groups, but it is not known whether they also function to minimize predation risk. Here, we show that crested macaques (Macaca nigra) react more strongly to playbacks of recruitment alarm calls (i.e. calls signalling the presence of a predator and eliciting cooperative mobbing behaviour) if they were produced by an individual with whom they share a strong social bond. Dominance relationships between caller and listener had no effect on the reaction of the listener. Thus, strong social bonds may improve the coordination and efficiency of cooperative defence against predators, and therefore increase chances of survival. This result broadens our understanding of the evolution and function of social bonds by highlighting their importance in the anti-predator context.

Facilitating play through communication: significance of teeth exposure in the gorilla play face.

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.

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.

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.