Chimpanzees use social information to acquire a skill they fail to innovate.

Cumulative cultural evolution has been claimed to be a uniquely human phenomenon pivotal to the biological success of our species. One plausible condition for cumulative cultural evolution to emerge is individuals' ability to use social learning to acquire know-how that they cannot easily innovate by themselves. It has been suggested that chimpanzees may be capable of such know-how social learning, but this assertion remains largely untested. Here we show that chimpanzees use social learning to acquire a skill that they failed to independently innovate. By teaching chimpanzees how to solve a sequential task (one chimpanzee in each of the two tested groups, n = 66) and using network-based diffusion analysis, we found that 14 naive chimpanzees learned to operate a puzzle box that they failed to operate during the preceding three months of exposure to all necessary materials. In conjunction, we present evidence for the hypothesis that social learning in chimpanzees is necessary and sufficient to acquire a new, complex skill after the initial innovation.

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.

Food sharing with friends and acquaintances: A study in preschool boys and girls.

Introduction: The current study examined whether preschoolers in a (semi-)natural situation shared more food with friends or acquaintances, and whether this was different between boys and girls, older and younger children, and for preferred and non- preferred food. In order to do so, we replicated and extended the classical work of Birch and Billman in a Dutch sample. Methods: Participants included 91 children aged between 3 to 6 years (52.7% boys, 93.4% Western European) from a middle- to upper-middle-class neighborhood in the Netherlands. Results: The results revealed that children shared more non-preferred than preferred food with others. Girls gave more non-preferred food to acquaintances than to friends, whereas boys gave more to friends than to acquaintances. No effect of relationship was found for preferred food. Older children shared more food than younger children. Compared to acquaintances, friends made more active attempts to get food. Moreover, children who were not shared with were just as likely to share food as children who were shared with. Discussion: Overall, only a small degree of agreement with the original study was found: Some significant findings could not be replicated, and some unconfirmed hypotheses of the original study were supported. The results underscore both the need for replications and studying the effect of social-contextual factors in natural settings.

Chimpanzee communities differ in their inter- and intrasexual social relationships.

Male and female human social bonding strategies are culturally shaped, in addition to being genetically rooted. Investigating nonhuman primate bonding strategies across sex groups allows researchers to assess whether, as with humans, they are shaped by the social environment or whether they are genetically predisposed. Studies of wild chimpanzees show that in some communities males have strong bonds with other males, whereas in others, females form particularly strong intrasex bonds, potentially indicative of cultural differences across populations. However, excluding genetic or ecological explanations when comparing different wild populations is difficult. Here, we applied social network analysis to examine male and female social bonds in two neighbouring semiwild chimpanzee groups of comparable ecological conditions and subspecies compositions, but that differ in demographic makeup. Results showed differences in bonding strategies across the two groups. While female-female party co-residence patterns were significantly stronger in Group 1 (which had an even distribution of males and females) than in Group 2 (which had a higher proportion of females than males), there were no such differences for male-male or male-female associations. Conversely, female-female grooming bonds were stronger in Group 2 than in Group 1. We also found that, in line with captive studies but contrasting research with wild chimpanzees, maternal kinship strongly predicted proximity and grooming patterns across the groups. Our findings suggest that, as with humans, male and female chimpanzee social bonds are influenced by the specific social group they live in, rather than predisposed sex-based bonding strategies.

Biased cultural transmission of a social custom in chimpanzees.

Cultural transmission studies in animals have predominantly focused on identifying between-group variation in tool-use techniques, while immaterial cultures remain understudied despite their potential for highlighting similarities between human and animal culture. Here, using long-term data from two chimpanzee communities, we tested whether one of chimpanzees' most enigmatic social customs-the grooming handclasp-is culturally transmitted by investigating the influence of well-documented human transmission biases on their variational preferences. After identifying differences in style preferences between the communities, we show that older and dominant individuals exert more influence over their partners' handclasp styles. Mothers were equally likely to influence their offspring's preferences as nonkin, indicating that styles are transmitted both vertically and obliquely. Last, individuals gradually converged on the group style, suggesting that conformity guides chimpanzees' handclasp preferences. Our findings show that chimpanzees' social lives are influenced by cultural transmission biases that hitherto were thought to be uniquely human.

Does tolerance allow bonobos to outperform chimpanzees on a cooperative task? A conceptual replication of Hare et al., 2007.

Across various taxa, social tolerance is thought to facilitate cooperation, and many species are treated as having species-specific patterns of social tolerance. Yet studies that assess wild and captive bonobos and chimpanzees result in contrasting findings. By replicating a cornerstone experimental study on tolerance and cooperation in bonobos and chimpanzees (Hare et al. 2007 Cur. Biol. 17, 619-623 (doi:10.1016/j.cub.2007.02.040)), we aim to further our understanding of current discrepant findings. We tested bonobos and chimpanzees housed at the same facility in a co-feeding and cooperation task. Food was placed on dishes located on both ends or in the middle of a platform. In the co-feeding task, the tray was simply made available to the ape duos, whereas in the cooperation task the apes had to simultaneously pull at both ends of a rope attached to the platform to retrieve the food. By contrast to the published findings, bonobos and chimpanzees co-fed to a similar degree, indicating a similar level of tolerance. However, bonobos cooperated more than chimpanzees when the food was monopolizable, which replicates the original study. Our findings call into question the interpretation that at the species level bonobos cooperate to a higher degree because they are inherently more tolerant.

Chimpanzees communicate to coordinate a cultural practice.

Human culture thrives by virtue of communication, yet whether communication plays an influential role in the cultural lives of other animals remains understudied. Here, we investigated whether chimpanzees use communication to engage in a cultural practice by analysing grooming handclasp (GHC) interactions-a socio-cultural behaviour requiring interindividual coordination for successful execution. Previous accounts attributed GHC initiations to behavioural shaping, whereby the initiator physically moulds the partner's arm into the desired GHC posture. Using frame-by-frame analysis and matched-control methodology, we find that chimpanzees do not only shape their partner's posture (22%), but also use gestural communication to initiate GHC (44%), which requires an active and synchronized response from the partner. Moreover, in a third (34%) of the GHC initiations, the requisite coordination was achieved by seemingly effortless synchrony. Lastly, using a longitudinal approach, we find that for GHC initiations, communication occurs more frequently than shaping in experienced dyads and less in mother-offspring dyads. These findings are consistent with ontogenetic ritualization, thereby reflecting first documentation of chimpanzees communicating to coordinate a cultural practice. We conclude that chimpanzees show interactional flexibility in the socio-cultural domain, opening the possibility that the interplay between communication and culture is rooted in our deep evolutionary history.

Chimpanzees organize their social relationships like humans.

Human relationships are structured in a set of layers, ordered from higher (intimate relationships) to lower (acquaintances) emotional and cognitive intensity. This structure arises from the limits of our cognitive capacity and the different amounts of resources required by different relationships. However, it is unknown whether nonhuman primate species organize their affiliative relationships following the same pattern. We here show that the time chimpanzees devote to grooming other individuals is well described by the same model used for human relationships, supporting the existence of similar social signatures for both humans and chimpanzees. Furthermore, the relationship structure depends on group size as predicted by the model, the proportion of high-intensity connections being larger for smaller groups.

Self-interest precludes prosocial juice provisioning in a free choice group experiment in bonobos.

Previous studies on prosociality in bonobos have reported contrasting results, which might partly be explained by differences in experimental contexts. In this study, we implement a free choice group experiment in which bonobos can provide fruit juice to their group members at a low cost for themselves. Four out of five bonobos passed a training phase and understood the setup and provisioned fruit juice in a total of 17 dyads. We show that even in this egalitarian group with a shallow hierarchy, the majority of pushing was done by the alpha female, who monopolized the setup and provided most juice to two adult females, her closest social partners. Nonetheless, the bonobos in this study pushed less frequently than the chimpanzees in the original juice-paradigm study, suggesting that bonobos might be less likely than chimpanzees to provide benefits to group members. Moreover, in half of the pushing acts, subjects obtained juice for themselves, suggesting that juice provisioning was partly driven by self-regarding behavior. Our study indicates that a more nuanced view on the prosocial food provisioning nature of bonobos is warranted but based on this case study, we suggest that the observed sex differences in providing food to friends corresponds with the socio-ecological sex difference in cooperative interactions in wild and zoo-housed bonobos.

Drivers of Dyadic Cofeeding Tolerance in Pan: A Composite Measure Approach.

This study aimed to construct a composite model of Dyadic Cofeeding Tolerance (DCT) in zoo-housed bonobos and chimpanzees using a validated experimental cofeeding paradigm and to investigate whether components resulting from this model differ between the two species or vary with factors such as sex, age, kinship and social bond strength. Using dimension reduction analysis on five behavioral variables from the experimental paradigm (proximity, aggression, food transfers, negative food behavior, participation), we found a two-factor model: "Tolerant Cofeeding" and "Agonistic Cofeeding". To investigate the role of social bond quality on DCT components alongside species effects, we constructed and validated a novel relationship quality model for bonobos and chimpanzees combined, resulting in two factors: Relationship Value and Incompatibility. Interestingly, bonobos and chimpanzees did not differ in DCT scores, and sex and kinship effects were identical in both species but biased by avoidance of the resource zone by male-male dyads in bonobos. Social bonds impacted DCT similarly in both species, as dyads with high Relationship Value showed more Tolerant Cofeeding, while dyads with higher Relationship Incompatibility showed more Agonistic Cofeeding. We showed that composite DCT models can be constructed that take into account both negative and positive cofeeding behavior. The resulting DCT scores were predicted by sex, kinship and social bonds in a similar fashion in both Pan species, likely reflecting their adaptability to changing socio-ecological environments. This novel operational measure to quantify cofeeding tolerance can now be applied to a wider range of species in captivity and the wild to see how variation in local socio-ecological circumstances influences fitness interdependence and cofeeding tolerance at the dyadic and group levels. This can ultimately lead to a better understanding of how local environments have shaped the evolution of tolerance in humans and other species.

Adult bonobos show no prosociality in both prosocial choice task and group service paradigm.

Previous studies reported contrasting conclusions concerning bonobo prosociality, which are likely due to differences in the experimental design, the social dynamics among subjects and characteristics of the subjects themselves. Two hypotheses have been proposed to explain the occurrence of prosociality in animals: the cooperative breeding hypothesis and the self-domestication hypothesis. While the former predicts low levels of prosociality in bonobos because they are non-cooperative breeders, the latter predicts high levels of prosociality because self-domestication has been proposed to select for high levels of tolerance in this species. Here, we presented a group of thirteen bonobos with two platform food-provisioning tasks: the prosocial choice task (PCT) and the group service paradigm (GSP). The latter has so far never been applied to bonobos. To allow for free choice of participation and partner, we implemented both tasks in a group setting. Like in previous PCT studies, bonobos did not choose the prosocial option more often when a group member could benefit vs not benefit. In the GSP, where food provisioning is costly, only subadult bonobos showed a limited amount of food provisioning, which was much lower than what was previously reported for chimpanzees. In both experiments, adult subjects were highly motivated to obtain rewards for themselves, suggesting that bonobos behaved indifferently to the gains of group members. We suggest that previous positive food-provisioning prosociality results in bonobos are mainly driven by the behaviour of subadult subjects. The lack of prosociality in this study corresponds to the hypothesis that proactive food provisioning co-occurs with cooperative breeding and suggests that proactive prosociality might not be part of the self-domestication syndrome in bonobos.

What isn't social tolerance? The past, present, and possible future of an overused term in the field of primatology.

In the past four decades, the term social tolerance has been utilized to describe, explain, and predict many different aspects of primates' sociality and has been measured with a large range of traits and behaviors. To date, however, there has been little discussion on whether these different phenomena all reflect one and the same construct. This paper opens the discussion by presenting the historical development of the term social tolerance and a structured overview of its current, overextended use. We argue that social tolerance has developed to describe two distinct concepts: social tolerance as the social structure of a group and social tolerance as the dyadic or group-level manifestation of tolerant behaviors. We highlight how these two concepts are based on conflicting theoretical understandings and practical assessments. In conclusion, we present suggestions for future research on primate social tolerance, which will allow for a more systematic and comparable investigation of primate sociality.

Early Trauma Leaves No Social Signature in Sanctuary-Housed Chimpanzees (Pan troglodytes).

Negative early experiences can have detrimental effects on social functioning in later life, both in humans as well as in other socially-living animals. In zoo-housed chimpanzees, recent evidence suggests that there may be a lingering signature of early trauma on individuals' social interaction tendencies as measured by social proximity and grooming. Here, we address whether a similar effect would be observable in chimpanzees living under semi-wild conditions in an African sanctuary. By analysing party size, close proximity and social grooming, we show that in this specific sanctuary, chimpanzees that suffered early trauma (n = 42) were socially indistinguishable from chimpanzees who were born and raised by their mothers in the sanctuary (n = 36). Our findings indicate that chimpanzees may not be irreversibly affected by early social trauma, possibly owing to rehabilitation in stable social groups in a semi-natural environment. Beyond identifying sanctuaries as valuable rehabilitation centres for orphaned chimpanzees, this study demonstrates a remarkable social flexibility in one of our closest living relatives.

Foraging zebra finches (Taeniopygia guttata) are public information users rather than conformists.

Social learning enables adaptive information acquisition provided that it is not random but selective. To understand species typical decision-making and to trace the evolutionary origins of social learning, the heuristics social learners use need to be identified. Here, we experimentally tested the nature of majority influence in the zebra finch. Subjects simultaneously observed two demonstrator groups differing in relative and absolute numbers (ratios 1 : 2/2 : 4/3 : 3/1 : 5) foraging from two novel food sources (black and white feeders). We find that demonstrator groups influenced observers' feeder choices (social learning), but that zebra finches did not copy the majority of individuals. Instead, observers were influenced by the foraging activity (pecks) of the demonstrators and in an anti-conformist fashion. These results indicate that zebra finches are not conformist, but are public information users.

Temporal stability of chimpanzee social culture.

Culture is a hallmark of the human species, both in terms of the transmission of material inventions (e.g. tool manufacturing) and the adherence to social conventions (e.g. greeting mannerisms). While material culture has been reported across the animal kingdom, indications of social culture in animals are limited. Moreover, there is a paucity of evidencing cultural stability in animals. Here, based on a large dataset spanning 12 years, I show that chimpanzees adhere to arbitrary group-specific handclasp preferences that cannot be explained by genetics or the ecological environment. Despite substantial changes in group compositions across the study period, and all chimpanzees having several behavioural variants in their repertoires, chimpanzees showed and maintained the within-group homogeneity and between-group heterogeneity that are so characteristic of the cultural phenomenon in the human species. These findings indicate that human culture, including its arbitrary social conventions and long-term stability, is rooted in our evolutionary history.

Beyond social learning.

Cultural evolution requires the social transmission of information. For this reason, scholars have emphasized social learning when explaining how and why culture evolves. Yet cultural evolution results from many mechanisms operating in concert. Here, we argue that the emphasis on social learning has distracted scholars from appreciating both the full range of mechanisms contributing to cultural evolution and how interactions among those mechanisms and other factors affect the output of cultural evolution. We examine understudied mechanisms and other factors and call for a more inclusive programme of investigation that probes multiple levels of the organization, spanning the neural, cognitive-behavioural and populational levels. To guide our discussion, we focus on factors involved in three core topics of cultural evolution: the emergence of culture, the emergence of cumulative cultural evolution and the design of cultural traits. Studying mechanisms across levels can add explanatory power while revealing gaps and misconceptions in our knowledge. This article is part of the theme issue 'Foundations of cultural evolution'.

Erratum: Cofeeding tolerance in chimpanzees depends on group composition: A longitudinal study across four communities.

[This corrects the article DOI: 10.1016/j.isci.2021.102175.].

Cofeeding tolerance in chimpanzees depends on group composition: a longitudinal study across four communities.

Social tolerance is generally treated as a stable, species-specific characteristic. Recent research, however, has questioned this position and emphasized the importance of intraspecific variation. We investigate the temporal stability of social tolerance in four groups of sanctuary-housed chimpanzees over eight years using a commonly employed measure: experimental cofeeding tolerance. We then draw on longitudinal data on the demographic composition of each group to identify the factors associated with cofeeding tolerance. We find appreciable levels of variation in cofeeding tolerance across both groups and years that correspond closely to changes in group-level demographic composition. For example, cofeeding tolerance is lower when there are many females with young infants. These results suggest that social tolerance may be a "responding trait" of chimpanzee sociality, reflecting individual-level behavioral responses to social changes. Additional, experimental research is needed to better model the causal drivers of social tolerance within and among species.

Chimpanzees behave prosocially in a group-specific manner.

Chimpanzees act cooperatively in the wild, but whether they afford benefits to others, and whether their tendency to act prosocially varies across communities, is unclear. Here, we show that chimpanzees from neighboring communities provide valuable resources to group members at personal cost, and that the magnitude of their prosocial behavior is group specific. Provided with a resource-donation experiment allowing free (partner) choice, we observed an increase in prosocial acts across the study period in most of the chimpanzees. When group members could profit (test condition), chimpanzees provided resources more frequently and for longer durations than when their acts produced inaccessible resources (control condition). Strikingly, chimpanzees' prosocial behavior was group specific, with more socially tolerant groups acting more prosocially. We conclude that chimpanzees may purposely behave prosocially toward group members, and that the notion of group-specific sociality in nonhuman animals should crucially inform discussions on the evolution of prosocial behavior.