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.

Scleral pigmentation leads to conspicuous, not cryptic, eye morphology in chimpanzees.

Gaze following has been argued to be uniquely human, facilitated by our depigmented, white sclera [M. Tomasello, B. Hare, H. Lehmann, J. Call, J. Hum. Evol. 52, 314-320 (2007)]-the pale area around the colored iris-and to underpin human-specific behaviors such as language. Today, we know that great apes show diverse patterns of scleral coloration [J. A. Mayhew, J. C. Gómez, Am. J. Primatol. 77, 869-877 (2015); J. O. Perea García, T. Grenzner, G. Hesková, P. Mitkidis, Commun. Integr. Biol. 10, e1264545 (2016)]. We compare scleral coloration and its relative contrast with the iris in bonobos, chimpanzees, and humans. Like humans, bonobos' sclerae are lighter relative to the color of their irises; chimpanzee sclerae are darker than their irises. The relative contrast between the sclera and iris in all 3 species is comparable, suggesting a perceptual mechanism to explain recent evidence that nonhuman great apes also rely on gaze as a social cue.

Can third-party observers detect attraction in others based on subtle nonverbal cues?

In a series of three studies, we examined whether third-party observers can detect attraction in others based on subtle nonverbal cues. We employed video segments of dates collected from a speed-dating experiment, in which daters went on a brief (approx. 4 min) blind-date and indicated whether they would like to go on another date with their brief interaction partner or not. We asked participants to view these stimuli and indicate whether or not each couple member is attracted to their partner. Our results show that participants could not reliably detect attraction, and this ability was not influenced by the age of the observer, video segment location (beginning or middle of the date), video duration, or general emotion recognition capacity. Contrary to previous research findings, our findings suggest that third-party observers cannot reliably detect attraction in others. However, there was one exception: Recognition rose above chance level when the daters were both interested in their partners compared to when they were not interested. Supplementary Information: The online version contains supplementary material available at 10.1007/s12144-022-02927-0.

The ontogeny of human laughter.

Human adult laughter is characterized by vocal bursts produced predominantly during exhalation, yet apes laugh while exhaling and inhaling. The current study investigated our hypothesis that laughter of human infants changes from laughter similar to that of apes to increasingly resemble that of human adults over early development. We further hypothesized that the more laughter is produced on the exhale, the more positively it is perceived. To test these predictions, novice (n = 102) and expert (phonetician, n = 15) listeners judged the extent to which human infant laughter (n = 44) was produced during inhalation or exhalation, and the extent to which they found the laughs pleasant and contagious. Support was found for both hypotheses, which were further confirmed in two pre-registered replication studies. Likely through social learning and the anatomical development of the vocal production system, infants' initial ape-like laughter transforms into laughter similar to that of adult humans over the course of ontogeny.

Hearing Status Affects Children's Emotion Understanding in Dynamic Social Situations: An Eye-Tracking Study.

OBJECTIVES: For children to understand the emotional behavior of others, the first two steps involve emotion encoding and emotion interpreting, according to the Social Information Processing model. Access to daily social interactions is prerequisite to a child acquiring these skills, and barriers to communication such as hearing loss impede this access. Therefore, it could be challenging for children with hearing loss to develop these two skills. The present study aimed to understand the effect of prelingual hearing loss on children's emotion understanding, by examining how they encode and interpret nonverbal emotional cues in dynamic social situations. DESIGN: Sixty deaf or hard-of-hearing (DHH) children and 71 typically hearing (TH) children (3-10 years old, mean age 6.2 years, 54% girls) watched videos of prototypical social interactions between a target person and an interaction partner. At the end of each video, the target person did not face the camera, rendering their facial expressions out of view to participants. Afterward, participants were asked to interpret the emotion they thought the target person felt at the end of the video. As participants watched the videos, their encoding patterns were examined by an eye tracker, which measured the amount of time participants spent looking at the target person's head and body and at the interaction partner's head and body. These regions were preselected for analyses because they had been found to provide cues for interpreting people's emotions and intentions. RESULTS: When encoding emotional cues, both the DHH and TH children spent more time looking at the head of the target person and at the head of the interaction partner than they spent looking at the body or actions of either person. Yet, compared with the TH children, the DHH children looked at the target person's head for a shorter time (b = -0.03, p = 0.030), and at the target person's body (b = 0.04, p = 0.006) and at the interaction partner's head (b = 0.03, p = 0.048) for a longer time. The DHH children were also less accurate when interpreting emotions than their TH peers (b = -0.13, p = 0.005), and their lower scores were associated with their distinctive encoding pattern. CONCLUSIONS: The findings suggest that children with limited auditory access to the social environment tend to collect visually observable information to compensate for ambiguous emotional cues in social situations. These children may have developed this strategy to support their daily communication. Yet, to fully benefit from such a strategy, these children may need extra support for gaining better social-emotional knowledge.

The Role of Emotion Projection, Sexual Desire, and Self-Rated Attractiveness in the Sexual Overperception Bias.

A consistent finding in the literature is that men overperceive sexual interest in women (i.e., sexual overperception bias). Several potential mechanisms have been proposed for this bias, including projecting one's own interest onto a given partner, sexual desire, and self-rated attractiveness. Here, we examined the influence of these factors in attraction detection accuracy during speed-dates. Sixty-seven participants (34 women) split in four groups went on a total of 10 speed-dates with all opposite-sex members of their group, resulting in 277 dates. The results showed that attraction detection accuracy was reliably predicted by projection of own interest in combination with participant sex. Specifically, men were more accurate than women in detecting attraction when they were not interested in their partner compared to when they were interested. These results are discussed in the wider context of arousal influencing detection of partner attraction.

Pupil mimicry promotes trust through the theory-of-mind network.

The human eye can provide powerful insights into the emotions and intentions of others; however, how pupillary changes influence observers' behavior remains largely unknown. The present fMRI-pupillometry study revealed that when the pupils of interacting partners synchronously dilate, trust is promoted, which suggests that pupil mimicry affiliates people. Here we provide evidence that pupil mimicry modulates trust decisions through the activation of the theory-of-mind network (precuneus, temporo-parietal junction, superior temporal sulcus, and medial prefrontal cortex). This network was recruited during pupil-dilation mimicry compared with interactions without mimicry or compared with pupil-constriction mimicry. Furthermore, the level of theory-of-mind engagement was proportional to individual's susceptibility to pupil-dilation mimicry. These data reveal a fundamental mechanism by which an individual's pupils trigger neurophysiological responses within an observer: when interacting partners synchronously dilate their pupils, humans come to feel reflections of the inner states of others, which fosters trust formation.

Pupil responses to dynamic negative facial expressions of emotion in infants and parents.

Observing others' emotions triggers physiological arousal in infants as well as in adults, reflected in dilated pupil sizes. This study is the first to examine parents' and infants' pupil responses to dynamic negative emotional facial expressions. Moreover, the links between pupil responses and negative emotional dispositions were explored among infants and parents. Infants' and one of their parent's pupil responses to negative versus neutral faces were measured via eye tracking in 222 infants (5- to 7-month-olds, n = 77, 11- to 13-month-olds, n = 78, and 17- to 19-month-olds, n = 67) and 229 parents. One parent contributed to the pupil data, whereas both parents were invited to fill in questionnaires on their own and their infant's negative emotional dispositions. Infants did not differentially respond to negative expressions, while parents showed stronger pupil responses to negative versus neutral expressions. There was a positive association between infants' and their parent's mean pupil responses and significant links between mothers' and fathers' stress levels and their infants' pupil responses. We conclude that a direct association between pupil responses in parents and offspring is observable already in infancy in typical development. Stress in parents is related to their infants' pupillary arousal to negative emotions.

Low relationship quality predicts scratch contagion during tense situations in orangutans (Pongo pygmaeus).

Primates show various forms of behavioral contagion that are stronger between kin and friends. As a result, behavioral contagion is thought to promote group coordination, social cohesion, and possibly state matching. Aside from contagious yawning, little is known about the contagious effect of other behaviors. Scratching is commonly observed during arousal and as such may play a role within group dynamics. While the Bornean orangutan (Pongo pygmaeus) is commonly considered the least social great ape, orangutans do engage in social interactions. Therefore, their social organization makes them a suitable case for studying the social function of behavioral contagion. Through behavioral observations of captive orangutans, we recorded all yawn and scratch events together with the corresponding behavior of all bystander group-members. As yawning was rarely observed, no conclusions could be drawn regarding this behavior. Scratching was contagious and occurred within 90 s after the triggering scratch. Specifically, orangutans showed increased scratch contagion when they had seen a weakly bonded individual scratch during tense contexts. When the orangutan had not seen the triggering scratch, the contagiousness of scratching was not affected by context or relationship quality. Our results indicate that behavioral contagion is not simply higher between individuals with stronger social relationships, but that the contagiousness of behaviors may vary based on the context and on social factors. We discuss these findings in light of an adaptive function that may reduce aggression.

Pupil mimicry in infants and parents.

Changes in pupil size can reflect social interest or affect, and tend to get mimicked by observers during eye contact. Pupil mimicry has recently been observed in young infants, whereas it is unknown whether the extent and the speed of infants' pupil mimicry response are identical to that of adults. Moreover, the question of whether pupil mimicry in infants is modulated by the race of the observed other remains to be explored. In two studies, pupil mimicry was investigated in infants and their parents. In the first study, 6-, 12- and 18-month-olds (n = 194) and their parents (n = 192) observed eyes with dynamically dilating, constricting, or static pupils. Infants mimicked the pupil sizes of the observed eyes like their parents, but responded slower. Study 2 replicated these findings in a new sample of infants (n = 55, 12-month-olds) and parents (n = 64), and further showed that the pupil mimicry response was not significantly modulated by the race of the observed partner neither in infants nor in parents. We conclude that pupil mimicry is an ancient bonding mechanism that helps to connect people.

Bonobos (Pan paniscus) show an attentional bias toward conspecifics' emotions.

In social animals, the fast detection of group members' emotional expressions promotes swift and adequate responses, which is crucial for the maintenance of social bonds and ultimately for group survival. The dot-probe task is a well-established paradigm in psychology, measuring emotional attention through reaction times. Humans tend to be biased toward emotional images, especially when the emotion is of a threatening nature. Bonobos have rich, social emotional lives and are known for their soft and friendly character. In the present study, we investigated (i) whether bonobos, similar to humans, have an attentional bias toward emotional scenes compared with conspecifics showing a neutral expression, and (ii) which emotional behaviors attract their attention the most. As predicted, results consistently showed that bonobos' attention was biased toward the location of the emotional versus neutral scene. Interestingly, their attention was grabbed most by images showing conspecifics such as sexual behavior, yawning, or grooming, and not as much-as is often observed in humans-by signs of distress or aggression. The results suggest that protective and affiliative behaviors are pivotal in bonobo society and therefore attract immediate attention in this species.

Looking into your eyes: observed pupil size influences approach-avoidance responses.

The eyes reveal important social messages, such as emotions and whether a person is aroused and interested or bored and fatigued. A growing body of research has also shown that individuals with large pupils are generally evaluated positively by observers, while those with small pupils are perceived negatively. Here, we examined whether observed pupil size influences approach-avoidance tendencies. Participants performed an Approach-Avoidance Task using faces with large and small pupil sizes. Results showed that pupil size influences the accuracy of arm movements. Specifically, individuals were less prone to approach a face with small pupils than a face with large pupils. Conversely, participants were less prone to avoid a face with large pupils than a face with small pupils. Collectively, these findings suggest that perceivers attend to a facial cue - pupil size - when interacting with others.

Preprocessing pupil size data: Guidelines and code.

Pupillometry has been one of the most widely used response systems in psychophysiology. Changes in pupil size can reflect diverse cognitive and emotional states, ranging from arousal, interest and effort to social decisions, but they are also widely used in clinical practice to assess patients' brain functioning. As a result, research involving pupil size measurements has been reported in practically all psychology, psychiatry, and psychophysiological research journals, and now it has found its way into the primatology literature as well as into more practical applications, such as using pupil size as a measure of fatigue or a safety index during driving. The different systems used for recording pupil size are almost as variable as its applications, and all yield, as with many measurement techniques, a substantial amount of noise in addition to the real pupillometry data. Before analyzing pupil size, it is therefore of crucial importance first to detect this noise and deal with it appropriately, even prior to (if need be) resampling and baseline-correcting the data. In this article we first provide a short review of the literature on pupil size measurements, then we highlight the most important sources of noise and show how these can be detected. Finally, we provide step-by-step guidelines that will help those interested in pupil size to preprocess their data correctly. These guidelines are accompanied by an open source MATLAB script (available at https://github.com/ElioS-S/pupil-size ). Given that pupil diameter is easily measured by standard eyetracking technologies and can provide fundamental insights into cognitive and emotional processes, it is hoped that this article will further motivate scholars from different disciplines to study pupil size.

The role of pupil size in communication. Is there room for learning?

The eyes are extremely important for communication. The muscles around the eyes express emotional states and the size of the pupil signals whether a person is aroused and alert or bored and fatigued. Pupil size is an overlooked social signal, yet is readily picked up by observers. Observers mirror their own pupil sizes in response, which can influence social impressions. In a landmark study by Hess [1975. The role of pupil size in communication. Scientific American, 233(5), 110-119] it was shown that individuals with large pupils are perceived more positively than individuals with small pupils. In that behavioral study, participants were asked to draw pupils in line drawings of faces with empty irises and they drew large pupils in the happy face, and small ones in the angry face. The current study tested 579 participants (aged 4-80 years old) and extended this work by showing that this association between large (small) pupils and a positive (negative) impression develops over age and is absent in children. Several explanations for how individuals through interactions with close others learn that large pupils mean care, interest and attention and small pupils the opposite, are discussed. To conclude, this study shows that pupil size and emotion perception are intertwined but that their relationship develops over age.

Recognition of facial expressions is moderated by Islamic cues.

Recognising emotions from faces that are partly covered is more difficult than from fully visible faces. The focus of the present study is on the role of an Islamic versus non-Islamic context, i.e. Islamic versus non-Islamic headdress in perceiving emotions. We report an experiment that investigates whether briefly presented (40 ms) facial expressions of anger, fear, happiness and sadness are perceived differently when covered by a niqab or turban, compared to a cap and shawl. In addition, we examined whether oxytocin, a neuropeptide regulating affection, bonding and cooperation between ingroup members and fostering outgroup vigilance and derogation, would differentially impact on emotion recognition from wearers of Islamic versus non-Islamic headdresses. The results first of all show that the recognition of happiness was more accurate when the face was covered by a Western compared to Islamic headdress. Second, participants more often incorrectly assigned sadness to a face covered by an Islamic headdress compared to a cap and shawl. Third, when correctly recognising sadness, they did so faster when the face was covered by an Islamic compared to Western headdress. Fourth, oxytocin did not modulate any of these effects. Implications for theorising about the role of group membership on emotion perception are discussed.

Pupil-mimicry conditions trust in partners: moderation by oxytocin and group membership.

Across species, oxytocin, an evolutionarily ancient neuropeptide, facilitates social communication by attuning individuals to conspecifics' social signals, fostering trust and bonding. The eyes have an important signalling function; and humans use their salient and communicative eyes to intentionally and unintentionally send social signals to others, by contracting the muscles around their eyes and pupils. In our earlier research, we observed that interaction partners with dilating pupils are trusted more than partners with constricting pupils. But over and beyond this effect, we found that the pupil sizes of partners synchronize and that when pupils synchronously dilate, trust is further boosted. Critically, this linkage between mimicry and trust was bound to interactions between ingroup members. The current study investigates whether these findings are modulated by oxytocin and sex of participant and partner. Using incentivized trust games with partners from ingroup and outgroup whose pupils dilated, remained static or constricted, this study replicates our earlier findings. It further reveals that (i) male participants withhold trust from partners with constricting pupils and extend trust to partners with dilating pupils, especially when given oxytocin rather than placebo; (ii) female participants trust partners with dilating pupils most, but this effect is blunted under oxytocin; (iii) under oxytocin rather than placebo, pupil dilation mimicry is weaker and pupil constriction mimicry stronger; and (iv) the link between pupil constriction mimicry and distrust observed under placebo disappears under oxytocin. We suggest that pupil-contingent trust is parochial and evolved in social species in and because of group life.

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.

No immediate attentional bias towards or choice bias for male secondary sexual characteristics in Bornean orang-utans (Pongo pygmaeus).

Primate faces provide information about a range of variant and invariant traits, including some that are relevant for mate choice. For example, faces of males may convey information about their health or genetic quality through symmetry or facial masculinity. Because perceiving and processing such information may have bearing on the reproductive success of an individual, cognitive systems are expected to be sensitive to facial cues of mate quality. However, few studies have investigated this topic in non-human primate species. Orang-utans are an interesting species to test mate-relevant cognitive biases, because they are characterised by male bimaturism: some adult males are fully developed and bear conspicuous flanges on the side of their face, while other males look relatively similar to females. Here, we describe two non-invasive computerised experiments with Bornean orang-utans (Pongo pygmaeus), testing (i) immediate attention towards large flanges and symmetrical faces using a dot-probe task (N = 3 individuals; 2F) and (ii) choice bias for pictures of flanged males over unflanged males using a preference test (N = 6 individuals; 4F). In contrast with our expectations, we found no immediate attentional bias towards either large flanges or symmetrical faces. In addition, individuals did not show a choice bias for stimuli of flanged males. We did find exploratory evidence for a colour bias and energy efficiency trade-offs in the preference task. We discuss our null results and exploratory results in the context of the evolutionary history of Bornean orang-utans, and provide suggestions for a more biocentric approach to the study of orang-utan cognition.