Sequence-based machine learning reveals 3D genome differences between bonobos and chimpanzees.

The 3D structure of the genome is an important mediator of gene expression. As phenotypic divergence is largely driven by gene regulatory variation, comparing genome 3D contacts across species can further understanding of the molecular basis of species differences. However, while experimental data on genome 3D contacts in humans is increasingly abundant, only a handful of 3D genome contact maps exist for other species. Here, we demonstrate that human experimental data can be used to close this data gap. We apply a machine learning model that predicts 3D genome contacts from DNA sequence to the genomes from 56 bonobos and chimpanzees and identify species-specific patterns of genome folding. We estimated 3D divergence between individuals from the resulting contact maps in 4,420 1 Mb genomic windows, of which ∼17% were substantially divergent in predicted genome contacts. Bonobos and chimpanzees diverged at 89 windows, overlapping genes associated with multiple traits implicated in Pan phenotypic divergence. We discovered 51 bonobo-specific variants that individually produce the observed bonobo contact pattern in bonobo-chimpanzee divergent windows. Our results demonstrate that machine learning methods can leverage human data to fill in data gaps across species, offering the first look at population-level 3D genome variation in non-human primates. We also identify loci where changes in 3D folding may contribute to phenotypic differences in our closest living relatives.

Deep genetic substructure within bonobos.

Establishing the genetic and geographic structure of populations is fundamental, both to understand their evolutionary past and preserve their future. Nevertheless, the patterns of genetic population structure are unknown for most endangered species. This is the case for bonobos (Pan paniscus), which, together with chimpanzees (Pan troglodytes), are humans' closest living relatives. Chimpanzees live across equatorial Africa and are classified into four subspecies,1 with some genetic population substructure even within subspecies. Conversely, bonobos live exclusively in the Democratic Republic of Congo and are considered a homogeneous group with low genetic diversity,2 despite some population structure inferred from mtDNA. Nevertheless, mtDNA aside, their genetic structure remains unknown, hampering our understanding of the species and conservation efforts. Mapping bonobo genetic diversity in space is, however, challenging because, being endangered, only non-invasive sampling is possible for wild individuals. Here, we jointly analyze the exomes and mtDNA from 20 wild-born bonobos, the whole genomes of 10 captive bonobos, and the mtDNA of 136 wild individuals. We identify three genetically distinct bonobo groups of inferred Central, Western, and Far-Western geographic origin within the bonobo range. We estimate the split time between the central and western populations to be ∼145,000 years ago and genetic differentiation to be in the order of that of the closest chimpanzee subspecies. Furthermore, our estimated long-term Ne for Far-West (∼3,000) is among the lowest estimated for any great ape lineage. Our results highlight the need to attend to the bonobo substructure, both in terms of research and conservation.

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.

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.

Water scooping: tool use by a wild bonobo (Pan paniscus) at LuiKotale, a case report.

Tool use diversity is often considered to differentiate our two closest living relatives: the chimpanzee (Pan troglodytes) and the bonobo (P. paniscus). Chimpanzees appear to have the largest repertoire of tools amongst nonhuman primates, and in this species, many forms of tool use enhance food and water acquisition. In captivity, bonobos seem as adept as chimpanzees in tool use complexity, including in the foraging context. However, in the wild, bonobos have only been observed engaging in habitual tool use in the contexts of comfort, play, self-directed behaviour and communication, whilst no tool-assisted food acquisition has been reported. Whereas captive bonobos use tools for drinking, so far, the only report from the wild populations comes down to four observations of moss sponges used at Lomako. Here, we present the first report of tool use in the form of water scooping by a wild bonobo at LuiKotale. An adult female was observed and videotaped whilst using an emptied Cola chlamydantha pod to scoop and drink water from a stream. We discuss the conditions for such observations and the importance of looking out for rare behaviours and attempt to put the observation into the context of the opportunity versus necessity hypotheses. By adding novel information on tool use, our report contributes to the ongoing efforts to differentiate population-specific traits in the behavioural ecology of the bonobo.

Chaotic image encryption algorithm with improved bonobo optimizer and DNA coding for enhanced security.

Image encryption involves applying cryptographic approaches to convert the content of an image into an illegible or encrypted format, reassuring that illegal users cannot simply interpret or access the actual visual details. Commonly employed models comprise symmetric key algorithms for the encryption of the image data, necessitating a secret key for decryption. This study introduces a new Chaotic Image Encryption Algorithm with an Improved Bonobo Optimizer and DNA Coding (CIEAIBO-DNAC) for enhanced security. The presented CIEAIBO-DNAC technique involves different processes such as initial value generation, substitution, diffusion, and decryption. Primarily, the key is related to the input image pixel values by the MD5 hash function, and the hash value produced by the input image can be utilized as a primary value of the chaotic model to boost key sensitivity. Besides, the CIEAIBO-DNAC technique uses the Improved Bonobo Optimizer (IBO) algorithm for scrambling the pixel position in the block and the scrambling process among the blocks takes place. Moreover, in the diffusion stage, DNA encoding, obfuscation, and decoding process were carried out to attain encrypted images. Extensive experimental evaluations and security analyses are conducted to assess the outcome of the CIEAIBO-DNAC technique. The simulation outcome demonstrates excellent security properties, including resistance against several attacks, ensuring it can be applied to real-time image encryption scenarios.

What we know and don't know about great ape cultural communication in the wild.

Following the first descriptions of culture in primates, widespread agreement has developed that the term can be applied to nonhumans as group-specific, socially learned behaviors. While behaviors such as those involving extractive tool use have been researched intensively, we propose that behaviors that are more subtle, less likely to be ecologically constrained, and more likely to be socially shaped, such as cultural forms of communication, provide compelling evidence of culture in nonhuman primates. Additionally, cultural forms of communication can provide novel insights into animal cognition such as the capacity for conformity, conventionalized meanings, arbitrariness in signal forms, and even symbolism. In this paper we focus on evidence from studies conducted on wild great apes. First, we provide a thorough review of what exactly we do know, and by extension don't know, about great ape cultural communication. We argue that detailed research on both vocal and gestural communication in wild great apes shows a more nuanced and variable repertoire than once assumed, with increasing support for group-specific variation. Second, we discuss the relevance of great ape cultural communication and its potential for illustrating evolutionary continuity for human-like cultural attributes, namely cumulative culture and symbolism. In sum, a concerted effort to examine cultural forms of communication in great apes could reveal novel evidence for cultural capacities that have thus far been heavily debated in the literature and can simultaneously contribute to an improved understanding of the complex minds of our closest living relatives.

An expedition in the jungle of pluripotent stem cells of non-human primates.

For nearly three decades, more than 80 embryonic stem cell lines and more than 100 induced pluripotent stem cell lines have been derived from New World monkeys, Old World monkeys, and great apes. In this comprehensive review, we examine these cell lines originating from marmoset, cynomolgus macaque, rhesus macaque, pig-tailed macaque, Japanese macaque, African green monkey, baboon, chimpanzee, bonobo, gorilla, and orangutan. We outline the methodologies implemented for their establishment, the culture protocols for their long-term maintenance, and their basic molecular characterization. Further, we spotlight any cell lines that express fluorescent reporters. Additionally, we compare these cell lines with human pluripotent stem cell lines, and we discuss cell lines reprogrammed into a pluripotent naive state, detailing the processes used to attain this. Last, we present the findings from the application of these cell lines in two emerging fields: intra- and interspecies embryonic chimeras and blastoids.

Visually assessed body condition shows high heritability in a pedigreed great ape population.

Body condition, a measure for relative fat mass, is associated with primate health, fitness, and overall welfare. Body condition is often influenced by dietary factors, age, and/or sex, but several body condition measures (body weight, weight-to-height ratios, and so on) also show high heritability across primate species, indicating a role of genetic effects. Although different measures for body condition exist, many require direct handling of animals, which is invasive, time-consuming, and expensive, making them impractical in wild and captive settings. Therefore, noninvasive visual body condition score (BCS) systems were developed for various animal species, including macaques and chimpanzees, to visually assess relative fat mass. Here we evaluate the utility of a visual BCS system in bonobos by assessing (1) inter-rater reliability, (2) links with body mass, a traditional hands-on measure of condition, and (3) the factors driving individual variation in BCS. We adapted the chimpanzee BCS system to rate 76 bonobos in 11 European zoos (92% of the adult population). Inter-rater reliability was high (s* = 0.948), BCSs were positively associated with body mass (ß = 0.075) and not predicted by diet, sex, or age, nor were they associated with a higher abundance of obesity-related diseases. Instead, BCSs showed high levels of heritability (h2 = 0.637), indicating that a majority of body condition variation in bonobos is attributable to genetic similarity of the individuals. This is in line with reported h2 -values for traditional body condition measures in primates and provides support for the reliability of visual BCS systems in great apes. The results of this study emphasize an often unanticipated role of genetics in determining primate body fat and health that has implications for the management of captive primates. Application of this tool in wild populations would aid to unravel environmental from genetic drivers of body condition variation in primates.

Reproductive inequality among males in the genus Pan.

Reproductive inequality, or reproductive skew, drives natural selection, but has been difficult to assess, particularly for males in species with promiscuous mating and slow life histories, such as bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although bonobos are often portrayed as more egalitarian than chimpanzees, genetic studies have found high male reproductive skew in bonobos. Here, we discuss mechanisms likely to affect male reproductive skew in Pan, then re-examine skew patterns using paternity data from published work and new data from the Kokolopori Bonobo Reserve, Democratic Republic of Congo and Gombe National Park, Tanzania. Using the multinomial index (M), we found considerable overlap in skew between the species, but the highest skew occurred among bonobos. Additionally, for two of three bonobo communities, but no chimpanzee communities, the highest ranking male had greater siring success than predicted by priority-of-access. Thus, an expanded dataset covering a broader demographic range confirms that bonobos have high male reproductive skew. Detailed comparison of data from Pan highlights that reproductive skew models should consider male-male dynamics including the effect of between-group competition on incentives for reproductive concessions, but also female grouping patterns and factors related to male-female dynamics including the expression of female choice. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Multi-feature fusion and improved BO and IGWO metaheuristics based models for automatically diagnosing the sleep disorders from sleep sounds.

A night of regular and quality sleep is vital in human life. Sleep quality has a great impact on the daily life of people and those around them. Sounds such as snoring reduce not only the sleep quality of the person but also reduce the sleep quality of the partner. Sleep disorders can be eliminated by examining the sounds that people make at night. It is a very difficult process to follow and treat this process by experts. Therefore, this study, it is aimed to diagnose sleep disorders using computer-aided systems. In the study, the used data set contains seven hundred sound data which has seven different sound class such as cough, farting, laugh, scream, sneeze, sniffle, and snore. In the model proposed in the study, firstly, the feature maps of the sound signals in the data set were extracted. Three different methods were used in the feature extraction process. These methods are MFCC, Mel-spectrogram, and Chroma. The features extracted in these three methods are combined. Thanks to this method, the features of the same sound signal extracted in three different methods are used. This increases the performance of the proposed model. Later, the combined feature maps were analyzed using the proposed New Improved Gray Wolf Optimization (NI-GWO), which is the improved version of the Improved Gray Wolf Optimization (I-GWO) algorithm, and the proposed Improved Bonobo Optimizer (IBO) algorithm, which is the improved version of the Bonobo Optimizer (BO). In this way, it is aimed to run the models faster, reduce the number of features, and obtain the most optimum result. Finally, Support Vector Machine (SVM) and k-nearest neighbors (KNN) supervised shallow machine learning methods were used to calculate the metaheuristic algorithms' fitness values. Different types of metrics such as accuracy, sensitivity, F1 etc., were used for the performance comparison. Using the feature maps optimized by the proposed NI-GWO and IBO algorithms, the highest accuracy value was obtained from the SVM classifier with 99.28% for both metaheuristic algorithms.

A Retrospective Review of Dental Care and Related Husbandry of Captive Great Apes Over 37 Years (1982-2019) at Milwaukee County Zoo.

Milwaukee County Zoo (MCZ) has cared for 25 lowland gorillas (Gorilla gorilla gorilla), 17 orangutans (Pongo pygmaeus) and 38 bonobos (Pan paniscus) since 1982. MCZ has one of the largest captive populations of bonobos in the world, with a current troop of 19 animals and historically as many as 24 in the troop. This article reviews the dental care provided to these animals from 1982-2019.

A skew in poo: Biases in primate fecal isotope analysis and recommendations for standardized sample preparation.

Feces are a treasure trove in the study of animal behavior and ecology. Stable carbon and nitrogen isotope analysis allows to assess the dietary niches of elusive primate species and primate breastfeeding behavior. However, some fecal isotope data may unwillingly be biased toward the isotope ratios of undigested plant matter, requiring more consistent sample preparation protocols. We assess the impact of this potential data skew in 114 fecal samples of wild bonobos (Pan paniscus) by measuring the isotope differences (Δ13 C, Δ15 N) between bulk fecal samples containing larger particles (>1 mm) and filtered samples containing only small particles (<1 mm). We assess the influence of fecal carbon and nitrogen content (ΔC:N) and sample donor age (subadult, adult) on the resulting Δ13 C, Δ15 N values (n = 228). Additionally, we measure the isotope ratios in three systematically sieved fecal samples of chimpanzees (Pan troglodytes verus), with particle sizes ranging from 20 µm to 8 mm (n = 30). We found differences in fecal carbon and nitrogen content, with the smaller fecal fraction containing more nitrogen on average. While the Δ13 C values were small and not affected by age or ΔC:N, the Δ15 N values were significantly influenced by fecal ΔC:N, possibly resulting from the differing proportions of undigested plant macroparticles. Significant relationships between carbon stable isotope ratios (δ13 C) values and %C in large fecal fractions of both age groups corroborated this assessment. Δ15 N values were significantly larger in adults than subadults, which should be of concern in isotope studies comparing adult females with infants to assess breastfeeding. We found a random variation of up to 3.0‰ in δ13 C and 2.0‰ in nitrogen stable isotope ratios within the chimpanzee fecal samples separated by particle sizes. We show that particle size influences isotope ratios and propose a simple, cost-effective filtration method for primate feces to exclude larger undigested food particles from the analysis, which can easily be adopted by labs worldwide.

Linked OXTR Variants Are Associated with Social Behavior Differences in Bonobos (Pan paniscus).

Single-nucleotide polymorphisms (SNPs) in forkhead box protein P2 (FOXP2) and oxytocin receptor (OXTR) genes have been associated with linguistic and social development in humans, as well as to symptom severity in autism spectrum disorder (ASD). Studying biobehavioral mechanisms in the species most closely related to humans can provide insights into the origins of human communication, and the impact of genetic variation on complex behavioral phenotypes. Here, we aimed to determine if bonobos (Pan paniscus) exhibit individual variation in FOXP2 and OXTR loci that have been associated with human social development and behavior. Although the ASD-related variants were reported in 13-41% of the human population, we did not find variation at these loci in our sample of 13 bonobos. However, we did identify a novel variant in bonobo FOXP2, as well as four novel variants in bonobo OXTR that were 17-184 base pairs from the human ASD variants. We also found the same linked, homozygous allelic combination across the 4 novel OXTR SNPs (homozygous TGTC) in 6 of the 13 bonobos, indicating that this combination may be under positive selection. When comparing the combined OXTR genotypes, we found significant group differences in social behavior; bonobos with zero copies of the TGTC combination were less social than bonobos with one copy of the TGTC combination. Taken together, our findings suggest that these OXTR variants may influence individual-level social behavior in bonobos and support the notion that linked genetic variants are promising risk factors for social communication deficits in humans.

Evaluating Self-Directed Behaviours and Their Association with Emotional Arousal across Two Cognitive Tasks in Bonobos (Pan paniscus).

Self-directed behaviours (SDBs) are widely used as markers of emotional arousal in primates, and are commonly linked to negative arousal, or are used as indicators of stress or poor welfare. However, recent studies suggest that not all SDBs have the same function. Moreover, lateralisation in the production of these behaviours has been suggested to be associated with emotional processing. Hence, a better understanding of the production and the asymmetry of these displacement behaviours is needed in a wider range of species in order to confirm their reliability as indicators of emotional arousal. In the current study, we experimentally evaluated the production and asymmetry of SDBs in zoo-housed bonobos during two cognitive touchscreen tasks. Overall, nose wipes were most commonly observed, followed by gentle self-scratches, and rough self-scratches. The rates of nose wipes and rough self-scratches increased with incorrect responses, suggesting that these behaviours indicate arousal and possibly frustration. Rough self-scratching was additionally more directed towards the left hemispace after incorrect responses. In contrast, gentle self-scratching increased after correct responses in one study, possibly linking it with positive arousal. We also tested if left-handed bonobos showed greater behavioural reactivity towards incorrect responses, but found no evidence to confirm this hypothesis. Our results shed light on potential different mechanisms behind separate SDBs. We therefore provide nuance to the use of SDBs as indicator of emotional arousal in bonobos.

Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species.

In most animals, males are considered more aggressive, in terms of frequency and intensity of aggressive behaviors, than their female peers. However, in several species this widespread male-biased aggression pattern is either extenuated, absent, or even sex-reversed. Studies investigating potential neuro-physiological mechanisms driving the selection for female aggression in these species have revealed an important, but not exclusive role of androgens in the expression of the observed sex-specific behavioral patterns. Two very closely related mammalian species that markedly differ in the expression and degree of sex-specific aggression are the two Pan species, where the chimpanzee societies are male-dominated while in bonobos sex-biased aggression patterns are alleviated. Using liquid chromatography-mass spectrometry (LC-MS) methods, we measured levels of plasma testosterone and androstenedione levels in male and female zoo-housed bonobos (N = 21; 12 females, 9 males) and chimpanzees (N = 41; 27 females, 14 males). Our results show comparable absolute and relative intersexual patterns of blood androgen levels in both species of Pan. Plasma testosterone levels were higher in males (bonobos: females: average 0.53 ± 0.30 ng/mL; males 6.70 ± 2.93 ng/mL; chimpanzees: females: average 0.40 ± 0.23 ng/mL; males 5.84 ± 3.63 ng/mL) and plasma androstenedione levels were higher in females of either species (bonobos: females: average 1.83 ± 0.87 ng/mL; males 1.13 ± 0.44 ng/mL; chimpanzees: females: average 1.84 ± 0.92 ng/mL; males 1.22 ± 0.55 ng/mL). The latter result speaks against a role of androstenedione in the mediation of heightened female aggression, as had been suggested based on studies in other mammal species where females are dominant and show high levels of female aggressiveness.

A comparison of faecal glucocorticoid metabolite concentration and gut microbiota diversity in bonobos (Pan paniscus).

Sex, age, diet, stress and social environment have all been shown to influence the gut microbiota. In several mammals, including humans, increased stress is related to decreasing gut microbial diversity and may differentially impact specific taxa. Recent evidence from gorillas shows faecal glucocorticoid metabolite concentration (FGMC) did not significantly explain gut microbial diversity, but it was significantly associated with the abundance of the family Anaerolineaceae. These patterns have yet to be examined in other primates, like bonobos (Pan paniscus). We compared FGMC to 16S rRNA amplicons for 202 bonobo faecal samples collected across 5 months to evaluate the impact of stress, measured with FGMC, on the gut microbiota. Alpha diversity measures (Chao's and Shannon's indexes) were not significantly related to FGMC. FGMC explained 0.80 % of the variation in beta diversity for Jensen-Shannon and 1.2% for weighted UniFrac but was not significant for unweighted UniFrac. We found that genus SHD-231, a member of the family Anaerolinaceae had a significant positive relationship with FGMC. These results suggest that bonobos are relatively similar to gorillas in alpha diversity and family Anaerolinaceae responses to FGMC, but different from gorillas in beta diversity. Members of the family Anaerolinaceae may be differentially affected by FGMC across great apes. FGMC appears to be context dependent and may be species-specific for alpha and beta diversity but this study provides an example of consistent change in two African apes. Thus, the relationship between physiological stress and the gut microbiome may be difficult to predict, even among closely related species.

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.

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.