Increased alertness and moderate ingroup cohesion in bonobos' response to outgroup cues.

In a number of species, including humans, perceived outgroup threat can promote ingroup cohesion. However, the distribution and selection history of this association across species with varied intergroup relations remains unclear. Using a sample of 8 captive groups (N = 43 individuals), we here tested whether bonobos, like chimpanzees, show more affiliative ingroup behaviour following perception of outgroup cues (unfamiliar male long-distance vocalisations). We used comparable methods to our previous study of captive chimpanzees, and found that, although weaker, there was an association for more frequent social grooming in response to the outgroup condition than the control condition, alongside more alert posture and increased self-directed behaviour. This provides preliminary evidence for an ancestral origin to the proximate association between outgroup cues and ingroup cohesion, at least prior to the Pan-Homo split, and suggests the presence of intergroup competition in our last common ancestor.

Selective and prolonged attention to emotional scenes in humans and bonobos.

Perceiving emotions in others is at the foundation of higher-order social cognition. The importance of emotions is evidenced by the fact that they receive prioritized attention at early stages of processing the environment in humans and some other primates. Nevertheless, we do not fully understand how emotion modulates attention over longer durations in primates, particularly in great apes. Bonobos, one of our closest relatives, stand out in emotion processing and regulation among great apes. This makes them an interesting comparison species and a valuable model for studying the evolution of emotion perception in hominids. We investigated how bonobos and humans spontaneously attend to emotionally valent scenes in a preferential looking task using eye-tracking. With Bayesian mixed modelling, we found that bonobos and humans generally looked longer at emotional scenes, mainly of conspecifics. Moreover, while bonobos did not have a bias toward emotional human scenes, humans sustained their attention toward bonobos playing, grooming and having sex. Furthermore, when exploring an immediate bias for emotions, humans showed a bias toward affiliative human scenes, and bonobos showed a bias away from bonobos-in-distress scenes. These findings suggest that emotions modulate attention at early and later attentional stages in bonobos, similar to humans.

Comparative analysis of intragroup intermale relationships: a study of wild bonobos (Pan paniscus) in Wamba, Democratic Republic of Congo and chimpanzees (Pan troglodytes) in Kalinzu Forest Reserve, Uganda.

Although chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) share a multi-male/multi-female societal organization and form male-philopatric groups, disparities in terms of male aggression and stability of temporary parties are thought to exist among them. However, existing research in bonobos has mainly focused on the high social status, prolonged receptivity, and characteristic sexual behaviors of females, leaving the behaviors of males understudied. Moreover, prior comparative studies on Pan suffer from methodological inconsistencies. This study addresses these gaps by employing a uniform observation method to explore party attendance and aggressive interactions among male bonobos in Wamba and male chimpanzees in Kalinzu. Unlike male chimpanzees, which exhibit dispersion in the absence of receptive females in the group, male bonobos showed a lesser degree of such dispersion. Although the overall frequency of aggressive interactions per observation unit did not significantly differ between the two species, the nature of these interactions varied. Notably, severe aggressive behaviors such as physical confrontations among adult males were absent in bonobos, with most aggression occurring between the sons of the two highest-ranking females. Additionally, in bonobos, females actively engaged in polyadic aggressive behavior as aggressors, while all instances of coalitionary aggression in chimpanzees originated from male aggressors. These findings underscore the substantial impact of female behaviors on the observed distinctions in male aggressive interactions between the two species.

Animal behavior: A tale of two apes.

A new paper shows that rates of aggression are higher, and rates of coalition formation are lower, among male bonobos than among male chimpanzees. These findings are noteworthy because they challenge the view that female bonobos' preferences for less aggressive males favored a reduction in male aggression and an increase in social tolerance.

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.

Differences in expression of male aggression between wild bonobos and chimpanzees.

Researchers investigating the evolution of human aggression look to our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), as valuable sources of comparative data.1,2 Males in the two species exhibit contrasting patterns: male chimpanzees sexually coerce females3,4,5,6,7,8 and sometimes kill conspecifics,9,10,11,12 whereas male bonobos exhibit less sexual coercion13,14 and no reported killing.13 Among the various attempts to explain these species differences, the self-domestication hypothesis proposes negative fitness consequences of male aggression in bonobos.2,15,16 Nonetheless, the extent to which these species differ in overall rates of aggression remains unclear due to insufficiently comparable observation methods.17,18,19,20,21,22,23 We used 14 community-years of focal follow data-the gold standard for observational studies24-to compare rates of male aggression in 3 bonobo communities at the Kokolopori Bonobo Reserve, Democratic Republic of Congo, and 2 chimpanzee communities at Gombe National Park, Tanzania. As expected, given that females commonly outrank males, we found that bonobos exhibited lower rates of male-female aggression and higher rates of female-male aggression than chimpanzees. Surprisingly, we found higher rates of male-male aggression among bonobos than chimpanzees even when limiting analyses to contact aggression. In both species, more aggressive males obtained higher mating success. Although our findings indicate that the frequency of male-male aggression does not parallel species difference in its intensity, they support the view that contrary to male chimpanzees, whose reproductive success depends on strong coalitions, male bonobos have more individualistic reproductive strategies.25.

Cooperation across social borders in bonobos.

Cooperation beyond familial and group boundaries is core to the functioning of human societies, yet its evolution remains unclear. To address this, we examined grooming, coalition, and food-sharing patterns in bonobos (Pan paniscus), one of our closest living relatives whose rare out-group tolerance facilitates interaction opportunities between groups. We show that, as in humans, positive assortment supports bonobo cooperation across borders. Bonobo cooperative attitudes toward in-group members informed their cooperative relationships with out-groups, in particular, forming connections with out-group individuals who also exhibited high cooperation tendencies. Our findings show that cooperation between unrelated individuals across groups without immediate payoff is not exclusive to humans and suggest that such cooperation can emerge in the absence of social norms or strong cultural dispositions.

Between-group cooperation in bonobos.

Bonobos provide insight into the origins of partner-specific cooperation in human groups.

Humans recognize affective cues in primate vocalizations: acoustic and phylogenetic perspectives.

Humans are adept at extracting affective information from vocalizations of humans and other animals. However, the extent to which human recognition of vocal affective cues of other species is due to cross-taxa similarities in acoustic parameters or the phylogenetic closeness between species is currently unclear. To address this, we first analyzed acoustic variation in 96 affective vocalizations, taken from agonistic and affiliative contexts, of humans and three other primates-rhesus macaques (Macaca mulatta), chimpanzees and bonobos (Pan troglodytes and Pan paniscus). Acoustic analyses revealed that agonistic chimpanzee and bonobo vocalizations were similarly distant from agonistic human voices, but chimpanzee affiliative vocalizations were significantly closer to human affiliative vocalizations, than those of bonobos, indicating a potential derived vocal evolution in the bonobo lineage. Second, we asked 68 human participants to categorize and also discriminate vocalizations based on their presumed affective content. Results showed that participants reliably categorized human and chimpanzee vocalizations according to affective content, but not bonobo threat vocalizations nor any macaque vocalizations. Participants discriminated all species calls above chance level except for threat calls by bonobos and macaques. Our results highlight the importance of both phylogenetic and acoustic parameter level explanations in cross-species affective perception, drawing a more complex picture to the origin of vocal emotions.

Great ape cognition is structured by stable cognitive abilities and predicted by developmental conditions.

Great ape cognition is used as a reference point to specify the evolutionary origins of complex cognitive abilities, including in humans. This research often assumes that great ape cognition consists of cognitive abilities (traits) that account for stable differences between individuals, which change and develop in response to experience. Here, we test the validity of these assumptions by assessing repeatability of cognitive performance among captive great apes (Gorilla gorilla, Pongo abelii, Pan paniscus, Pan troglodytes) in five tasks covering a range of cognitive domains. We examine whether individual characteristics (age, group, test experience) or transient situational factors (life events, testing arrangements or sociality) influence cognitive performance. Our results show that task-level performance is generally stable over time; four of the five tasks were reliable measurement tools. Performance in the tasks was best explained by stable differences in cognitive abilities (traits) between individuals. Cognitive abilities were further correlated, suggesting shared cognitive processes. Finally, when predicting cognitive performance, we found stable individual characteristics to be more important than variables capturing transient experience. Taken together, this study shows that great ape cognition is structured by stable cognitive abilities that respond to different developmental conditions.

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'.

Hierarchical object combination and tool use in the great apes and human children.

Object manipulation can be used as a comparative scale of cognitive development among primates, including humans. Combinatory object manipulation is a precursor of tool-using behavior that indicates material intelligence in primates. However, developmental data on it regarding the great apes other than chimpanzees is insufficient. We conducted a longitudinal investigation of humans and chimpanzees as well as a cross-sectional examination of other great-ape infants (two bonobos, three gorillas, and four orangutans) in captive settings by using two kinds of tasks that required either inserting or stacking combinatory action. The four species of great apes and humans demonstrated both types of combinatory object manipulation during infancy. However, the order of development in different types of combinatory object manipulations varied among the great apes. Furthermore, we applied a nesting-cup task to examine the hierarchical complexity in the combinatory strategies of human children and adult chimpanzees. Both of them exhibited highly hierarchical combinations in the nesting-cup task and employed the subassembly strategy, indicating that an action merge may exist not only in human children but also in adult chimpanzees. The results were discussed with reviews of the tool-use literature from the wild great apes. The early acquisition of an inserting action in the chimpanzees may explain the tool utilization commonality reported in wild chimpanzees. The combinatory object manipulation may have worked as an external enhancer to achieve an additional hierarchical complexity in cognition and behavior, eventually leading humans to develop a language system.

Characterization of Pan social systems reveals in-group/out-group distinction and out-group tolerance in bonobos.

Human between-group interactions are highly variable, ranging from violent to tolerant and affiliative. Tolerance between groups is linked to our unique capacity for large-scale cooperation and cumulative culture, but its evolutionary origins are understudied. In chimpanzees, one of our closest living relatives, predominantly hostile between-group interactions impede cooperation and information flow across groups. In contrast, in our other closest living relative, the bonobo, tolerant between-group associations are observed. However, as these associations can be frequent and prolonged and involve social interactions that mirror those within groups, it is unclear whether these bonobos really do belong to separate groups. Alternatively, the bonobo grouping patterns may be homologous to observations from the large Ngogo chimpanzee community, where individuals form within-group neighborhoods despite sharing the same membership in the larger group. To characterize bonobo grouping patterns, we compare the social structure of the Kokolopori bonobos with the chimpanzee group of Ngogo. Using cluster analysis, we find temporally stable clusters only in bonobos. Despite the large spatial overlap and frequent interactions between the bonobo clusters, we identified significant association preference within but not between clusters and a unique space use of each cluster. Although bonobo associations are flexible (i.e., fission-fusion dynamics), cluster membership predicted the bonobo fission compositions and the spatial cohesion of individuals during encounters. These findings suggest the presence of a social system that combines clear in-group/out-group distinction and out-group tolerance in bonobos, offering a unique referential model for the evolution of tolerant between-group interactions in humans.

Manipulative repertoire of bonobos (Pan paniscus) in spontaneous feeding situation.

Comparative behavioral studies of hand use amongst primate species, including humans, have been central in research on evolutionary mechanisms. In particular, the manipulative abilities of our closest relatives, the chimpanzee (Pan troglodytes), have been widely described in various contexts, showing a high level of dexterity both in zoo and in natural conditions. In contrast, the study of bonobos' manipulative abilities has almost exclusively been carried out in experimental contexts related to tool use. The objective of the present study is to describe the richness of the manipulative repertoire of zoo-housed bonobos, in a spontaneous feeding context including various physical substrates to gain a larger insight into our evolutionary past. Our study describes a great variety of grasping postures and grip associations in bonobos, close to the range of manipulative repertoire in chimpanzees, confirming that the two species are not markedly different in terms of cognitive and morphological constraints associated with food manipulation. We also observed differences in manipulative behaviors between juveniles and adults, indicating a greater diversity in grip associations and grasping postures used in isolation with age, and a sex-biased use of tools with females using tools more often than males. These results are consistent with the previous results in the Pan genus and reinforce the hypothesis that the evolutionary mechanisms underlying the flexibility of manipulative behaviors are shared by both species and that these ecological strategies would have already evolved in their common ancestor.

Sex and grooming as exchange commodities in female bonobos' daily biological market.

The Biological Market Theory (BMT) posits that cooperation between non-human animals can be seen as a mutually beneficial exchange of commodities similarly to what observed in human economic markets. Positive social interactions are commodities in non-human animals, and mutual exchanges fulfilling the criteria of the BMT have been shown in several species. However, the study of biological markets suffers from methodological limitations that are mainly linked to the difficulty of clearly identifying the currencies and their exchanges in the short-term. Here, we test whether bonobo females are more attractive during their maximum swelling phase, whether they exchange grooming and Genito-Genital Rubbing (GGR) on a daily level of analysis, and whether these daily exchanges fulfil the BMT criteria. Females engaged more in GGR when their sexual swelling was in the maximum phase. Moreover, they exchanged grooming and sex according to the daily "market fluctuations" associated with swelling status. Females in the minimum phase (low-value) increased their probability to engage in GGR with females in the maximum phase (high-value) by grooming them preferentially. In line with the supply/demand law, the female grooming strategy varied depending on the daily number of swollen females present: the higher the number of swollen females, the lower the individual grooming preference. As a whole, our study confirms BMT as a valid model to explain daily commodity exchanges as a function of the temporary value of traders, and underlines the importance of a day-by-day approach to unveil the presence of a biological market when the value of traders frequently changes.

Attractiveness of female sexual signaling predicts differences in female grouping patterns between bonobos and chimpanzees.

Here we show that sexual signaling affects patterns of female spatial association differently in chimpanzees and bonobos, indicating its relevance in shaping the respective social systems. Generally, spatial association between females often mirrors patterns and strength of social relationships and cooperation within groups. While testing for proposed differences in female-female associations underlying female coalition formation in the species of the genus Pan, we find only limited evidence for a higher female-female gregariousness in bonobos. While bonobo females exhibited a slightly higher average number of females in their parties, there is neither a species difference in the time females spent alone, nor in the number of female party members in the absence of sexually attractive females. We find that the more frequent presence of maximally tumescent females in bonobos is associated with a significantly stronger increase in the number of female party members, independent of variation in a behavioural proxy for food abundance. This indicates the need to look beyond ecology when explaining species differences in female sociality as it refutes the idea that the higher gregariousness among bonobo females is driven by ecological factors alone and highlights that the temporal distribution of female sexual receptivity is an important factor to consider when studying mammalian sociality.

Time-lag of urinary and salivary cortisol response after a psychological stressor in bonobos (Pan paniscus).

Cortisol is often measured as a marker for stress. Therefore, a profound validation of the time-lag between the stressor and the increase and peak in cortisol levels is needed. No study measured both the urinary and salivary cortisol time-lag after a psychological stressor. In this study, we used a frequent sampling study design to (1) describe the urinary and salivary cortisol pattern during a control day; and (2) characterize the induced excretion pattern of urinary and salivary cortisol after a psychological stressor in six zoo-housed bonobos. Liquid chromatography-tandem mass spectrometry was used to analyze 71 urine and 162 saliva samples collected on a control and a test day. We found that the time-lag between the stressor and the maximal cortisol concentration was similar in urine and saliva (160 min after the stressor). However, salivary cortisol after the stressor did show a faster and steeper increase than urinary cortisol. We also show inter-individual variation in the baseline and stress levels of cortisol, which should be considered in future cortisol studies. Our research highlights the importance of validation studies to confirm relevant sampling windows for cortisol sampling in order to obtain biologically meaningful results.

Involuntary autobiographical memories and their relation to other forms of spontaneous thoughts.

Involuntary autobiographical memories are memories of personal events that come to mind spontaneously-that is, with no conscious initiation of the retrieval process. Such spontaneously arising memories were long ignored in cognitive psychology, which generally has focused on controlled and strategic forms of remembering, studied in laboratory settings. Recent evidence shows that involuntary memories of past events are highly frequent in daily life, and that they represent a context-sensitive, and associative way of recollecting past events that involves little executive control. They operate by constraints that favour recent events and events with a distinct feature overlap to the current situation, which optimizes the probability of functional relevance to the ongoing situation. In addition to adults, they are documented in young children and great apes and may be an ontogenetic and evolutionary forerunner of strategic retrieval of past events. Findings suggest that intrusive involuntary memories observed clinically after traumatic events should be viewed as a dysfunctional subclass of otherwise functional involuntary autobiographical memories. Because of their highly constrained, situation-dependent and automatic nature, involuntary autobiographical memories form a distinct category of spontaneous thought that cannot be equated with mind wandering. This article is part of the theme issue 'Offline perception: voluntary and spontaneous perceptual experiences without matching external stimulation'.

Mirror replication of sexual facial expressions increases the success of sexual contacts in bonobos.

Rapid Facial Mimicry (RFM), one of the possible predictors of emotional contagion, is defined as the rapid, involuntary and automatic replication of a facial expression. Up to now, RFM has been demonstrated in nonhuman animals exclusively during play. Since in bonobos, as in humans, socio-sexuality is a powerful tool for assessing/strengthening inter-individual relationships, we investigated RFM in this domain. Bonobos displayed silent bared-teeth (sbt, the most common facial expression during sexual contacts) more frequently after the detection of an sbt emitted by the trigger than in the no-detection condition. This is the first demonstration of the presence of RFM during sex. The occurrence of RFM was positively affected by the sex of the partners with female homo-sexual contacts being punctuated by a higher presence of RFM. At an immediate level, RFM increased the duration of homo- and hetero-sexual contacts. This finding suggests that RFM can increase individuals' potential fitness benefits. By prolonging their sexual contacts, females can strengthen their social relationships thus increasing the probability to obtain priority over resources (RFM indirect fitness benefits). Via longer copulations, males can increase the probability to make females pregnant (RFM direct fitness benefits). In conclusion, in bonobos the access to the partner's face during sexual contacts (face-to-face, proximate factor) and the role of socio-sexuality in increasing the individual direct and indirect fitness (ultimate factor) could have favoured the evolution of specific sexual facial expressions and their rapid mirror replication. Our findings on bonobos expand the role of RFM well beyond the animal play domain thus opening new scenarios for future comparative studies exploring the evolution of socio-sexuality in humans.