The expression of empathy in human's closest relatives, bonobos and chimpanzees: current and future directions.

Empathy is a complex, multi-dimensional capacity that facilitates the sharing and understanding of others' emotions. As our closest living relatives, bonobos (Pan paniscus) and chimpanzees (P. troglodytes) provide an opportunity to explore the origins of hominin social cognition, including empathy. Despite certain assumptions that bonobos and chimpanzees may differ empathically, these species appear to overlap considerably in certain socio-emotional responses related to empathy. However, few studies have systematically tested for species variation in Pan empathic or socio-emotional tendencies. To address this, we synthesise the growing literature on Pan empathy to inform our understanding of the selection pressures that may underlie the evolution of hominin empathy, and its expression in our last common ancestor. As bonobos and chimpanzees show overlaps in their expression of complex socio-emotional phenomena such as empathy, we propose that group comparisons may be as or more meaningful than species comparisons when it comes to understanding the evolutionary pressures for such behaviour. Furthermore, key differences, such as how humans and Pan communicate, appear to distinguish how we experience empathy compared to our closest living relatives.

Perceptual integration of bodily and facial emotion cues in chimpanzees and humans.

For highly visual species like primates, facial and bodily emotion expressions play a crucial role in emotion perception. However, most research focuses on facial expressions, while the perception of bodily cues is still poorly understood. Using a novel comparative priming eye-tracking design, we examined whether our close primate relatives, the chimpanzees (Pan troglodytes), and humans infer emotions from bodily cues through subsequent perceptual integration with facial expressions. In experiment 1, we primed chimpanzees with videos of bodily movements of unfamiliar conspecifics engaged in social activities of opposite valence (play and fear) against neutral control scenes to examine attentional bias toward succeeding congruent or incongruent facial expressions. In experiment 2, we assessed the same attentional bias in humans yet using stimuli showing unfamiliar humans. In experiment 3, humans watched the chimpanzee stimuli of experiment 1, to examine cross-species emotion perception. Chimpanzees exhibited a persistent fear-related attention bias but did not associate bodily with congruent facial cues. In contrast, humans prioritized conspecifics' congruent facial expressions (matching bodily scenes) over incongruent ones (mismatching). Nevertheless, humans exhibited no congruency effect when viewing chimpanzee stimuli, suggesting difficulty in cross-species emotion perception. These results highlight differences in emotion perception, with humans being greatly affected by fearful and playful bodily cues and chimpanzees being strongly drawn toward fearful expressions, regardless of the preceding bodily priming cue. These data advance our understanding of the evolution of emotion signaling and the presence of distinct perceptual patterns in hominids.

Group-specific expressions of co-feeding tolerance in bonobos and chimpanzees preclude dichotomous species generalizations.

Bonobos are typically portrayed as more socially tolerant than chimpanzees, yet the current evidence supporting such a species-level categorization is equivocal. Here, we used validated group-level co-feeding assays to systematically test expressions of social tolerance in sixteen groups of zoo- and sanctuary-housed bonobos and chimpanzees. We found that co-feeding tolerance substantially overlaps between the species, thus precluding categorical inference at the species level. Instead, marked differences were observed between groups, with some bonobo communities exhibiting higher social tolerance than chimpanzee communities, and vice versa. Moreover, considerable intergroup variation was found within species living in the same environment, which attests to Pan's behavioral flexibility. Lastly, chimpanzees showed more tolerance in male-skewed communities, whereas bonobos responded less pronounced to sex-ratio variation. We conclude that the pervasive dichotomy between the tolerant bonobo and the belligerent chimpanzee requires quantitative nuance, and that accurate phylogenetic tracing of (human) social behavior warrants estimations of intraspecific group variation.

The Association Between the Bared-Teeth Display and Social Dominance in Captive Chimpanzees (Pan troglodytes).

Humans use smiles - widely observed emotional expressions - in a variety of social situations, of which the meaning varies depending on social relationship and the context in which it is displayed. The homologue of the human smile in non-human primates - both due to morphological and functional similarities - is the bared-teeth display (BT). According to the power asymmetry hypothesis (PAH), species with strict linear dominance hierarchies are predicted to produce distinct communicative signals to avoid escalations of social conflicts. Hence, while the BT in a despotic species is predicted to be expressed from low- to high-ranking individuals, signaling submission, the BT in a tolerant species is predicted to be expressed in multiple contexts, regardless of rank. We tested this hypothesis in a group of 8 captive chimpanzees (Pan troglodytes), a species commonly characterized as rather despotic. An investigation of 11,774 dyadic social interactions revealed this chimpanzee group to have a linear dominance hierarchy, with moderate steepness. A Bayesian GLMM - used to test the effects of social contexts and rank relationships of dyads on the use of the BT display - indicated multi-contextual use of the BT which is contingent on the rank relationship. We also found that slight morphological and/or acoustic variants (i.e., silent bared-teeth and vocalized bared-teeth) of the BT display may have different communicative meanings. Our findings are in line with the prediction derived from the PAH for a moderately despotic species, and the view that the human smile originated from the primate BT display. Supplementary Information: The online version contains supplementary material available at 10.1007/s42761-022-00138-1.

Flexible signalling strategies by victims mediate post-conflict interactions in bonobos.

Compared to other animals, humans supposedly excel at voluntarily controlling and strategically displaying emotional signals. Yet, new data shows that nonhuman great apes' emotion expressions may also be subject to voluntary control. A key context to further explore this is during post-conflict (PC) periods, where signalling by distressed victims may influence bystander responses, including the offering of consolation. To address this, our study investigates the signalling behaviour of sanctuary-living bonobo victims following aggression and its relation to audience composition and PC interactions. Results show that the production of paedomorphic signals by victims (regardless of age) increased their chances of receiving consolation. In adults, the production of such signals additionally reduced the risk of renewed aggression from opponents. Signal production also increased with audience size, yet strategies differed by age: while immatures reduced signalling in proximity of close-social partners, adults did so especially after receiving consolation. These results suggest that bonobos can flexibly adjust their emotion signalling to influence the outcome of PC events, and that this tendency has a developmental trajectory. Overall, these findings highlight the potential role that flexible emotion communication played in the sociality of our last common ancestor with Pan. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Bared-teeth displays in bonobos (Pan paniscus): An assessment of the power asymmetry hypothesis.

Facial expressions are key to navigating social group life. The Power Asymmetry Hypothesis of Motivational Emancipation predicts that the type of social organization shapes the meaning of communicative displays in relation to an individual's dominance rank. The bared-teeth (BT) display represents one of the most widely observed communicative signals across primate species. Studies in macaques indicate that the BT display in despotic species is often performed unidirectionally, from low- to high-ranking individuals (signaling submission), whereas the BT display in egalitarian species is usually produced irrespective of dominance (mainly signaling affiliation and appeasement). Despite its widespread presence, research connecting BT displays to the power asymmetry hypothesis outside the Macaca genus remains scarce. To extend this knowledge, we investigated the production of BT in relation to social dominance in dyadic interactions (N = 11,377 events) of 11 captive bonobos (Pan paniscus). Although adult bonobos were more despotic than previously suggested in the literature, BT displays were produced irrespective of dominance rank. Moreover, while adults produced the BT exclusively during socio-sexual interactions, especially during periods of social tension, immature bonobos produced the BT in a wider number of contexts. As such, the results indicate that the communicative meaning of the BT display is consistent with signaling appeasement, especially in periods of social tension. Moreover, the BT display does not seem to signal social status, supporting the prediction for species with a high degree of social tolerance. These results advance our understanding of the origins of communicative signals and their relation to species' social systems.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Anthropomorphism in comparative affective science: Advocating a mindful approach.

Anthropomorphism is the attribution of human-like capacities and traits to non-human entities. Anthropomorphism is ubiquitous in everyday life and in scientific domains, operating both implicitly and explicitly as a function of the human lens through which we view the world. A rich history of work in psychology, animal behavior, cognitive science, and philosophy has highlighted the negative and, to a lesser degree, the positive implications of anthropomorphism. In this article, we aim to provide a nuanced perspective of how anthropomorphism impacts the work of comparative affective science. Specifically, we discuss three domains of empirical inquiry in which lessons can be drawn about the benefits and pitfalls of anthropomorphism: responses to death, inequity aversion, and prosocial behavior. On balance, we advocate a mindful approach to anthropomorphizing in comparative affective science, and comparative science more generally.

Emotional expressions in human and non-human great apes.

Humans and great apes are highly social species, and encounter conspecifics throughout their daily lives. During social interactions, they exchange information about their emotional states via expressions through different modalities including the face, body and voice. In this regard, their capacity to express emotions, intentionally or unintentionally, is crucial for them to successfully navigate their social worlds and to bond with group members. Darwin (1872) stressed similarities in how humans and other animals express their emotions, particularly with the great apes. Here, we show that emotional expressions have many conserved, yet also a number of divergent features. Some theorists consider emotional expressions as direct expressions of internal states, implying that they are involuntary, cannot be controlled and are inherently honest. Others see them as more intentional and/ or as indicators of the actor's future behavior. After reviewing the human and ape literature, we establish an integrative, evolutionary perspective and provide evidence showing that these different viewpoints are not mutually exclusive. Recent insights indicate that, in both apes and humans, some emotional expressions can be controlled or regulated voluntarily, including in the presence of audiences, suggesting modulation by cognitive processes. However, even non-intentional expressions such as pupil dilation can nevertheless inform others and influence future behavior. In sum, while showing deep evolutionary homologies across closely related species, emotional expressions show relevant species variation.

Response to Garcia and Dunn.

Garcia and Dunn [1] raise some interesting and valuable points regarding our recent paper in Current Biology[2]. As Garcia and Dunn [1] point out, cross-species variation in vocal and anatomical relations allows for the identification of relevant outliers from the body size - fundamental frequency (f0) regression. However, this depends on the premise that the chosen or available f0 and body size values are typical of the species. A motivation for our study [2] was in part to improve the accuracy of such estimates by providing more data per species compared to previous studies. We address each point of their critique by controlling for cross-species body size variation using body weights for chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), addressing potential call variation in different subspecies of Pan troglodytes, measuring minimum f0 as well as maximum f0 and possible effects caused by different larynx fixation methods.

Higher fundamental frequency in bonobos is explained by larynx morphology.

Acoustic signals, shaped by natural and sexual selection, reveal ecological and social selection pressures [1]. Examining acoustic signals together with morphology can be particularly revealing. But this approach has rarely been applied to primates, where clues to the evolutionary trajectory of human communication may be found. Across vertebrate species, there is a close relationship between body size and acoustic parameters, such as formant dispersion and fundamental frequency (f0). Deviations from this acoustic allometry usually produce calls with a lower f0 than expected for a given body size, often due to morphological adaptations in the larynx or vocal tract [2]. An unusual example of an obvious mismatch between fundamental frequency and body size is found in the two closest living relatives of humans, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although these two ape species overlap in body size [3], bonobo calls have a strikingly higher f0 than corresponding calls from chimpanzees [4]. Here, we compare acoustic structures of calls from bonobos and chimpanzees in relation to their larynx morphology. We found that shorter vocal fold length in bonobos compared to chimpanzees accounted for species differences in f0, showing a rare case of positive selection for signal diminution in both bonobo sexes.

What drives young children to over-imitate? Investigating the effects of age, context, action type, and transitivity.

Imitation underlies many traits thought to characterize our species, which includes the transmission and acquisition of language, material culture, norms, rituals, and conventions. From early childhood, humans show an intriguing willingness to imitate behaviors, even those that have no obvious function. This phenomenon, known as "over-imitation," is thought to explain some of the key differences between human cultures as compared with those of nonhuman animals. Here, we used a single integrative paradigm to simultaneously investigate several key factors proposed to shape children's over-imitation: age, context, transitivity, and action type. We compared typically developing children aged 4-6years in a task involving actions verbally framed as being instrumental, normative, or communicative in function. Within these contexts, we explored whether children were more likely to over-imitate transitive versus intransitive actions and manual versus body part actions. Results showed an interaction between age and context; as children got older, they were more likely to imitate within a normative context, whereas younger children were more likely to imitate in instrumental contexts. Younger children were more likely to imitate transitive actions (actions on objects) than intransitive actions compared with older children. Our results show that children are highly sensitive to even minimal cues to perceived context and flexibly adapt their imitation accordingly. As they get older, children's imitation appears to become less object bound, less focused on instrumental outcomes, and more sensitive to normative cues. This shift is consistent with the proposal that over-imitation becomes increasingly social in its function as children move through childhood and beyond.

Is Overimitation a Uniquely Human Phenomenon? Insights From Human Children as Compared to Bonobos.

Imitation is a key mechanism of human culture and underlies many of the intricacies of human social life, including rituals and social norms. Compared to other animals, humans appear to be special in their readiness to copy novel actions as well as those that are visibly causally irrelevant. This study directly compared the imitative behavior of human children to that of bonobos, our understudied great ape relatives. During an action-copying task involving visibly causally irrelevant actions, only 3- to 5-year-old children (N = 77) readily copied, whereas no bonobo from a large sample did (N = 46). These results highlight the distinctive nature of the human cultural capacity and contribute important insights into the development and evolution of human cultural behaviors.

A Comparison Between Bonobos and Chimpanzees: A Review and Update.

Chimpanzees (Pan troglodytes) and bonobos (P. paniscus) are our closest living relatives, with the human lineage diverging from the Pan lineage only around five to seven Mya, but possibly as early as eight Mya.1-2 Chimpanzees and bonobos even share genetic similarities with humans that they do not share with each other.2 Given their close genetic relationship to humans, both Pan species represent crucial living models for reconstructing our last common ancestor (LCA) and identifying uniquely human features. Comparing the similarities and differences of the two Pan is thus essential for constructing balanced models of human evolution.3.

Bonobos (Pan paniscus) vocally protest against violations of social expectations.

Research has shown that great apes possess certain expectations about social regularities and both perceive and act according to social rules within their group. During natural and experimentally induced contexts, such as the inequitable distribution of resources, individuals also show protesting behaviors when their expectations about a social situation are violated. Despite broad interest in this topic, systematic research examining the nature of these expectations and the communicative signals individuals use to express them remains scant. Here, we addressed this by exploring whether bonobos (Pan paniscus) respond to violations of social expectations in naturally occurring social interactions, focusing on the vocal behavior of victims following socially expected and unexpected aggression. Expected aggression included conflicts over a contested resource and conflicts that were provoked by the victim. Unexpected aggression was any spontaneous, unprovoked hostility toward the victim. For each conflict, we also determined its severity and the composition of the nearby audience. We found that the acoustic and temporal structure of victim screams was individually distinct and varied significantly depending on whether or not aggression could be socially predicted. Certain acoustic parameters also varied as a function of conflict severity, but unlike social expectation, conflict severity did not discriminate scream acoustic structure overall. We found no effect of audience composition. We concluded that, beyond the physical nature of a conflict, bonobos possess certain social expectations about how they should be treated and will publicly protest with acoustically distinctive vocal signals if these expectations are violated.

Functional flexibility in wild bonobo vocal behaviour.

A shared principle in the evolution of language and the development of speech is the emergence of functional flexibility, the capacity of vocal signals to express a range of emotional states independently of context and biological function. Functional flexibility has recently been demonstrated in the vocalisations of pre-linguistic human infants, which has been contrasted to the functionally fixed vocal behaviour of non-human primates. Here, we revisited the presumed chasm in functional flexibility between human and non-human primate vocal behaviour, with a study on our closest living primate relatives, the bonobo (Pan paniscus). We found that wild bonobos use a specific call type (the "peep") across a range of contexts that cover the full valence range (positive-neutral-negative) in much of their daily activities, including feeding, travel, rest, aggression, alarm, nesting and grooming. Peeps were produced in functionally flexible ways in some contexts, but not others. Crucially, calls did not vary acoustically between neutral and positive contexts, suggesting that recipients take pragmatic information into account to make inferences about call meaning. In comparison, peeps during negative contexts were acoustically distinct. Our data suggest that the capacity for functional flexibility has evolutionary roots that predate the evolution of human speech. We interpret this evidence as an example of an evolutionary early transition away from fixed vocal signalling towards functional flexibility.

Young children make their gestural communication systems more language-like: segmentation and linearization of semantic elements in motion events.

Research on Nicaraguan Sign Language, created by deaf children, has suggested that young children use gestures to segment the semantic elements of events and linearize them in ways similar to those used in signed and spoken languages. However, it is unclear whether this is due to children's learning processes or to a more general effect of iterative learning. We investigated whether typically developing children, without iterative learning, segment and linearize information. Gestures produced in the absence of speech to express a motion event were examined in 4-year-olds, 12-year-olds, and adults (all native English speakers). We compared the proportions of gestural expressions that segmented semantic elements into linear sequences and that encoded them simultaneously. Compared with adolescents and adults, children reshaped the holistic stimuli by segmenting and recombining their semantic features into linearized sequences. A control task on recognition memory ruled out the possibility that this was due to different event perception or memory. Young children spontaneously bring fundamental properties of language into their communication system.