The proximate regulation of prosocial behaviour: towards a conceptual framework for comparative research.

Humans and many other animal species act in ways that benefit others. Such prosocial behaviour has been studied extensively across a range of disciplines over the last decades, but findings to date have led to conflicting conclusions about prosociality across and even within species. Here, we present a conceptual framework to study the proximate regulation of prosocial behaviour in humans, non-human primates and potentially other animals. We build on psychological definitions of prosociality and spell out three key features that need to be in place for behaviour to count as prosocial: benefitting others, intentionality, and voluntariness. We then apply this framework to review observational and experimental studies on sharing behaviour and targeted helping in human children and non-human primates. We show that behaviours that are usually subsumed under the same terminology (e.g. helping) can differ substantially across and within species and that some of them do not fulfil our criteria for prosociality. Our framework allows for precise mapping of prosocial behaviours when retrospectively evaluating studies and offers guidelines for future comparative work.

A first exploratory comparison of the behaviour of wolves (Canis lupus) and wolf-dog hybrids in captivity.

Extensive introgression of genes from domesticated taxa may be a serious threat for the genomic integrity and adaptability of wild populations. Grey wolves (Canis lupus) are especially vulnerable to this phenomenon, but there are no studies yet assessing the potential behavioural effects of dog-introgression in wolves. In this study, we conducted a first systematic comparison of admixed (N = 11) and non-admixed (N = 14) wolves in captivity, focusing on their reaction to unfamiliar humans and novel objects, and the cohesiveness of their social groups. When exposed to unfamiliar humans in the experimental task, wolves were more vigilant, fearful and aggressive than admixed wolves, and less likely to approach humans, but also more likely to spend time in human proximity. When exposed to novel objects, wolves were more aggressive than admixed wolves, less likely to spend time in object proximity, and more likely to interact with objects, but also less vigilant and as fearful as admixed wolves. Finally, social networks were more cohesive in wolves than in admixed wolves. Although caution is needed when comparing groups of captive individuals with different life experiences, our study suggests that dog admixture may lead to important behavioural changes in wolves, with possible implications for conservation strategies.

Gestural communication in wild spider monkeys (Ateles geoffroyi).

Gestures play a central role in the communication systems of several animal families, including primates. In this study, we provide a first assessment of the gestural systems of a Platyrrhine species, Geoffroy's spider monkeys (Ateles geoffroyi). We observed a wild group of 52 spider monkeys and assessed the distribution of visual and tactile gestures in the group, the size of individual repertoires and the intentionality and effectiveness of individuals' gestural production. Our results showed that younger spider monkeys were more likely than older ones to use tactile gestures. In contrast, we found no inter-individual differences in the probability of producing visual gestures. Repertoire size did not vary with age, but the probability of accounting for recipients' attentional state was higher for older monkeys than for younger ones, especially for gestures in the visual modality. Using vocalizations right before the gesture increased the probability of gesturing towards attentive recipients and of receiving a response, although age had no effect on the probability of gestures being responded. Overall, our study provides first evidence of gestural production in a Platyrrhine species, and confirms this taxon as a valid candidate for research on animal communication.

Understanding others' preferences: A comparison across primate species and human societies.

We investigated children's and non-human great apes' ability to anticipate others' choices from their evident food preferences-regardless of whether these preferences deviate or align with one's own. We assessed children from three culturally-diverse societies (Namibia, Germany, and Samoa; N = 71; age range = 5-11) and four non-human great ape species (chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla gorilla), and orangutans (Pongo abelii); N = 25; age range = 7-29) regarding their choices in a dyadic food-retrieval task. Across conditions, participants' preferences were either aligned (same preference condition) or opposed (opposite preference condition) to those of their competitors. Children across societies altered their choices based on their competitor's preferences, indicating a cross-culturally recurrent capacity to anticipate others' choices relying on preferences-based inferences. In contrast to human children, all non-human great apes chose according to their own preferences but independent of those of their competitors. In sum, these results suggest that the tendency to anticipate others' choices based on their food preferences is cross-culturally robust and, among the great apes, most likely specific to humans.

A longitudinal comparison of maternal behaviour in German urban humans (Homo sapiens) and captive chimpanzees (Pan troglodytes).

Comparative perspectives are crucial in the study of human development, yet longitudinal comparisons of humans and other primates are still relatively uncommon. Here, we combined theoretical frameworks from cross-cultural and comparative psychology, to study maternal style in 10 mother-infant pairs of German urban humans (Homo sapiens) and 10 mother-infant pairs of captive chimpanzees (Pan troglodytes), during the first year of infants' development. We conducted focal observations of different behaviours (i.e. nursing, carrying, body contact, touching, grooming, restraining, approaching, leaving, rejection, aggression, mutual gaze, object stimulation), during natural interactions. Analyses revealed a more distal maternal style in WEIRD humans than in captive chimpanzees, with different behaviours being generally more common in one of the two species throughout development. For other behaviours (i.e. nursing), developmental trajectories differed between WEIRD humans and captive chimpanzees, although differences generally decreased through infants' development. Overall, our study confirms functional approaches as a valid tool for comparative longitudinal studies.

Maternal Investment Fosters Male but Not Female Social Interactions with Other Group Members in Immature Wild Spider Monkeys (Ateles geoffroyi).

In several species, individuals form long-lasting social relationships with other group members, which provide them with important fitness benefits. In primates, patterns of social relationships are known to differ between sexes, but little is known about how these differences emerge through development or the role that mothers might have in this process. Here, we investigated how sex differences in social behaviour emerge during the first six years of primate life and how sex-biased maternal investment can foster immatures' social development and social interaction with other group members. For this purpose, we observed 20 males and females aged between zero and six years in a wild group of spider monkeys (Ateles geoffroyi) that was male-philopatric and, therefore, expected to show sex-biased maternal investment. Our results showed no sex difference in the social development of offspring with regards to body contact and grooming, but the probability of play was rather constant throughout age for females, whereas, for males, it became higher than females around two years of age, peaking between three and four years of age. Moreover, we found differences between female and male immatures in the importance of maternal investment (which included the time mothers spent nursing, carrying, grooming, touching and playing with their offspring) for their social integration in the natal group. In particular, maternal investment increased the probability of playing with other group members for sons, but not for daughters. Our findings suggest that mothers, through sex-biased maternal investment, might have a crucial function in the social development of spider monkeys, fostering the abilities that young offspring need to thrive as adults. By shedding light on maternal investment and social development in a still understudied primate species, these findings contribute to understanding the evolutionary roots of human maternal care and social development.

Face to face interactions in chimpanzee (Pan troglodytes) and human (Homo sapiens) mother-infant dyads.

Human mothers interact with their infants in different ways. In Western, educated, industrialized, rich and democratic (WEIRD) societies, face-to-face interactions and mutual gazes are especially frequent, yet little is known about their developmental trajectories and if they differ from those of other primates. Using a cross-species developmental approach, we compared mother-infant interactions in 10 dyads of urban humans from a WEIRD society (Homo sapiens) and 10 dyads of captive zoo-based chimpanzees (Pan troglodytes), when infants were one, six and 12 months old. Results showed that face-to-face interactions with mutual gaze events were common in both groups throughout the infant's first year of life. The developmental trajectories of maternal and infants' looks partially differed between species, but mutual gaze events were overall longer in humans than in chimpanzees. Mutual gazes were also more frequent in humans, peaking at six months in humans, while increasing with age in chimpanzees. The duration and frequency of mutual gazes varied across contexts in both groups, with mutual gazes being longer during caring/grooming and feeding contexts. These findings confirm that some aspects of early socio-cognitive development are shared by humans and other primates, and highlight the importance of combining developmental and cross-species approaches to better understand the evolutionary roots of parenting behaviour. This article is part of a discussion meeting issue 'Face2face: advancing the science of social interaction'.

Primates unleashed.

Before claiming major differences between the communication systems of humans and other species, it is necessary to (1) overcome methodological limitations in the comparative study of communicative intentions; (2) account for mechanisms other than epistemic vigilance that may also sustain complex forms of communication; and (3) better differentiate between motivational and cognitive factors potentially affecting the emergence of open-ended communication.

Maternal and offspring behavior in free-ranging Japanese and moor macaques: A comparative approach.

Female primates represent the most important social partner for their developing offspring. However, mothers may strongly differ in the way they relate to their offspring (e.g., in terms of two different dimensions: protectiveness and rejection). In this study, we aimed to assess how dominance style predicts (i) changes in maternal behavior through offspring development, and (ii) the link between maternal behavior and offspring behavior. We conducted behavioral observations on 34 free-ranging immatures of two species of macaques with different dominance styles: less tolerant Japanese macaques (JM; Macaca fuscata) and more tolerant moor macaques (MM; Macaca maura). Our results showed that maternal behavior differed between JM and MM: maternal proximity and grooming decreased through offspring development more quickly in MM than in JM, whereas maternal rejection and aggression, which were generally more frequent in JM, decreased with offspring age similarly in both species. In contrast, maternal restraint of offspring decreased similarly with offspring age in both species. Furthermore, dominance style was differentially associated with the link between maternal and offspring behavior: in MM only, maternal grooming predicted an increase of the probability that offspring interacted with partners other than their mothers and engaged in solitary play, whereas maternal rejection predicted a decrease in the occurrence of solitary play. Overall, these results suggest interspecific variation in maternal behavior during offspring's first years of life, and point to the possibility that these differences may have an important role in shaping their behavioral development.

The social dynamics of complex gestural communication in great and lesser apes (Pan troglodytes, Pongo abelii, Symphalangus syndactylus).

Gestures play an essential role in primate communication. However, little is known about how complexity of gestural use (in terms of repertoire size, intentional use, flexibility and use of gestural sequences) relates to individual and dyadic measures of sociality and whether more complex gestural use is more effective in eliciting a response. We observed 19 captive chimpanzees (Pan troglodytes), 16 Sumatran orangutans (Pongo abelii) and 18 siamangs (Symphalangus syndactylus) to assess the complexity and effectiveness of their gestural use. We found that, beyond interspecies variation, the number of gesture types used in a dyad was higher when individuals had stronger social bonds; the probability of accounting for others' attention increased with age, especially for visual gestures; and sequences were more likely used by younger or socially less integrated individuals. In terms of effectiveness, older individuals and those using fewer sequences were more likely to be responded to, while across dyads, the probability of obtaining a response was higher when both individuals accounted for the other's attention and when they used fewer sequences. Overall, this confirms the link between sociality and complex gestural use and suggests that more complex forms of communication, at least in terms of intentional use, may be more effective at achieving communicative goals. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Great ape communication as contextual social inference: a computational modelling perspective.

Human communication has been described as a contextual social inference process. Research into great ape communication has been inspired by this view to look for the evolutionary roots of the social, cognitive and interactional processes involved in human communication. This approach has been highly productive, yet it is partly compromised by the widespread focus on how great apes use and understand individual signals. This paper introduces a computational model that formalizes great ape communication as a multi-faceted social inference process that integrates (a) information contained in the signals that make up an utterance, (b) the relationship between communicative partners and (c) the social context. This model makes accurate qualitative and quantitative predictions about real-world communicative interactions between semi-wild-living chimpanzees. When enriched with a pragmatic reasoning process, the model explains repeatedly reported differences between humans and great apes in the interpretation of ambiguous signals (e.g. pointing or iconic gestures). This approach has direct implications for observational and experimental studies of great ape communication and provides a new tool for theorizing about the evolution of uniquely human communication. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Attentional Bias to Facial Expressions of Different Emotions - A Cross-Cultural Comparison of ≠Akhoe Hai||om and German Children and Adolescents.

The attentional bias to negative information enables humans to quickly identify and to respond appropriately to potentially threatening situations. Because of its adaptive function, the enhanced sensitivity to negative information is expected to represent a universal trait, shared by all humans regardless of their cultural background. However, existing research focuses almost exclusively on humans from Western industrialized societies, who are not representative for the human species. Therefore, we compare humans from two distinct cultural contexts: adolescents and children from Germany, a Western industrialized society, and from the ≠Akhoe Hai||om, semi-nomadic hunter-gatherers in Namibia. We predicted that both groups show an attentional bias toward negative facial expressions as compared to neutral or positive faces. We used eye-tracking to measure their fixation duration on facial expressions depicting different emotions, including negative (fear, anger), positive (happy), and neutral faces. Both Germans and the ≠Akhoe Hai||om gazed longer at fearful faces, but shorter on angry faces, challenging the notion of a general bias toward negative emotions. For happy faces, fixation durations varied between the two groups, suggesting more flexibility in the response to positive emotions. Our findings emphasize the need for placing research on emotion perception into an evolutionary, cross-cultural comparative framework that considers the adaptive significance of specific emotions, rather than differentiating between positive and negative information, and enables systematic comparisons across participants from diverse cultural backgrounds.

Object preferences in captive Sumatran orang-utans (Pongo abelii).

While preferences for perceptual features of objects are well studied in humans, little is known about this trait in other great apes. We therefore presented captive Sumatran orang-utans (Pongo abelii) with objects that differed in shape (spherical, cuboid), colour (red, green), or texture (hard, soft). Overall, orang-utans preferred spherical over cuboid and red over green objects. Soft objects were preferred over hard ones. However, this preference might be confounded by the decomposable characteristic of soft objects since the orang-utans often unwrapped them. This study shows object preferences in orang-utans similar to those in humans, suggesting that perceptual preferences for basic object features such as shape and colour may be shared across primate species.

Disseminating Intention: How a term has spread within cross-species comparative science.

The current study takes a holistic view of cross-species comparative research and investigates the dissemination of the term intention as representative of the so-called "cognitive revolution." All references from 641 articles, published from 1948 to 2017, are used to analyze a citation network. The analysis visualizes and identifies prominent articles in the scientific debate and locates them structurally on a map. Each article is categorized in terms of the school of thought, its position within the discourse (e.g., opposing, supporting), the order of intentionality (e.g., 1st or 2nd order), and the species under consideration. By using a mixed-methods approach, which combines qualitative and quantitative methods, we identified 2 divergent schools of thought (psychological/philosophical and biological/behavioristic). Both schools introduced intention mostly independently from each other and show little overlap in citation habits. Both notions of intention have influenced comparative science until today. However, although the term finds limited application in various schools, only in connection with more cognitive approaches has it enjoyed a successful career, as indicated by the increasing number of articles in which it is used. Most controversy does not surround the concept of intention itself but its order. Furthermore, taking account of which species are investigated could reveal a pronounced primate bias in past discourse. Articles on nonprimate species using the term intention in the cognitive sense are markedly outnumbered by those on primates. The study reminds comparative psychologists of the importance to integrate a historical perspective into current debates, to avoid "speciesism" and talking past each other. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

A stepping stone to compositionality in chimpanzee communication.

Compositionality refers to a structural property of human language, according to which the meaning of a complex expression is a function of the meaning of its parts and the way they are combined. Compositionality is a defining characteristic of all human language, spoken and signed. Comparative research into the emergence of human language aims at identifying precursors to such key features of human language in the communication of other primates. While it is known that chimpanzees, our closest relatives, produce a variety of gestures, facial expressions and vocalizations in interactions with their group members, little is known about how these signals combine simultaneously. Therefore, the aim of the current study is to investigate whether there is evidence for compositional structures in the communication of chimpanzees. We investigated two semi-wild groups of chimpanzees, with focus on their manual gestures and their combinations with facial expressions across different social contexts. If there are compositional structures in chimpanzee communication, adding a facial expression to a gesture should convey a different message than the gesture alone, a difference that we expect to be measurable by the recipient's response. Furthermore, we expect context-dependent usage of these combinations. Based on a form-based coding procedure of the collected video footage, we identified two frequently used manual gestures (stretched arm gesture and bent arm gesture) and two facial expression (bared teeth face and funneled lip face). We analyzed whether the recipients' response varied depending on the signaler's usage of a given gesture + face combination and the context in which these were used. Overall, our results suggest that, in positive contexts, such as play or grooming, specific combinations had an impact on the likelihood of the occurrence of particular responses. Specifically, adding a bared teeth face to a gesture either increased the likelihood of affiliative behavior (for stretched arm gesture) or eliminated the bias toward an affiliative response (for bent arm gesture). We show for the first time that the components under study are recombinable, and that different combinations elicit different responses, a property that we refer to as componentiality. Yet our data do not suggest that the components have consistent meanings in each combination-a defining property of compositionality. We propose that the componentiality exhibited in this study represents a necessary stepping stone toward a fully evolved compositional system.

How primates acquire their gestures: evaluating current theories and evidence.

Mechanisms underlying gesture acquisition in primates are largely unstudied, yet heavily debated. While some studies suggest that gestural repertoires are largely innate, others emphasize that gestures emerge and are shaped in social interactions with other conspecifics. There is agreement, however, regarding the negligible role of imitation for the acquisition of gestures. The aim of this paper is to provide an overview of the current knowledge about gesture acquisition in nonhuman primates, to introduce the corresponding mechanisms suggested to be involved, and to discuss how findings from current studies support the different theories of gesture acquisition. We suggest that seemingly inconsistent findings across different research groups can be reconciled by pointing to differences between their research foci as well as methods of data collection. The additional comparison of the developmental pathways of gestural and facial communication highlights the complex interplay of genetic as well as social factors involved in shaping a species repertoire. We close by proposing that extending longitudinal studies, which capture the onset and usage of gestures in young primates, and which include the comparisons of several species and groups in different environments, will enable us to better understand developmental pathways of gestural communication in primates.

Conflict resolution in socially housed Sumatran orangutans (Pongo abelii).

BACKGROUND: Peaceful conflict resolution strategies have been identified as effective mechanisms for minimising the potential costs of group life in many gregarious species, especially in primates. The knowledge of conflict-management in orangutans, though, is still extremely limited. Given their semi-solitary lives in the wild, there seems to be barely a need for orangutans to apply conflict management strategies other than avoidance. However, because of the rapid loss of orangutan habitat due to deforestation, opportunities to prevent conflicts by dispersion are shrinking. Additionally, more and more orangutans are brought into rehabilitation centres where they are bound to live in close contact with conspecifics. This raises the questions of whether and how orangutans are able to cope with conflicts, which are inevitably connected with group life. METHODS: Observational zoo-studies provide a valuable method to investigate such potential: in zoos, orangutans usually live in permanent groups and face the challenges of group life every day. Therefore, we observed a group of six socially-housed Sumatran orangutans at the Dortmund Zoo, Germany, both in their spacious outdoor enclosure in the summer and in the less spacious indoor enclosure in the winter. During 157.5 h of observation, we collected data on aggressive interactions, third-party interventions and post-conflict affiliations. We applied the post-conflict/matched-control observation (PC/MC) and the time rule method to investigate the occurrence of reconciliation and post-conflict third-party affiliations. RESULTS: We recorded a total of 114 aggressive interactions (including conflicts in the context of weaning and of male sexual coercion). As expected, we found an increase of both open conflicts and peaceful conflict resolution under less spacious conditions. In accordance with previous reports, we observed interventions by initially uninvolved individuals. Whereas we found no clear evidence for post-conflict third-party affiliations, we were able to demonstrate the occurrence of reconciliation among orangutans. DISCUSSION: Notwithstanding the small sample size and the explorative character of our study, we found evidence that orangutans possess a potential for prosocial conflict resolution. When living in groups and under conditions in which dispersion is no longer an option, orangutans are capable to flexibly apply strategies of conflict resolution to cease open conflicts and to repair the potential social damage of aggressive interactions. These strategies are similar to those of other great apes.

Different Approaches to Meaning in Primate Gestural and Vocal Communication.

In searching for the roots of human language, comparative researchers investigate whether precursors to language are already present in our closest relatives, the non-human primates. As the majority of studies into primates' communication use a unimodal approach with focus on one signal type only, researchers investigate very different aspects depending on whether they are interested in vocal, gestural, or facial communication. Here, we focus on two signal types and discuss how meaning is created in the gestural (visual, tactile/auditory) as compared to the vocal modality in non-human primates, to highlight the different research foci across these modalities. First, we briefly describe the defining features of meaning in human language and introduce some debates concerning meaning in non-human communication. Second, with focus on these features, we summarize the current evidence for meaningful communication in gestural as compared to vocal communication and demonstrate that meaning is operationalized very differently by researchers in these two fields. As a result, it is currently not possible to generalize findings across these modalities. Rather than arguing for or against the occurrence of semantic communication in non-human primates, we aim at pointing to gaps of knowledge in studying meaning in our closest relatives, and these gaps might be closed.

The goal of ape pointing.

Captive great apes regularly use pointing gestures in their interactions with humans. However, the precise function of this gesture is unknown. One possibility is that apes use pointing primarily to direct attention (as in "please look at that"); another is that they point mainly as an action request (such as "can you give that to me?"). We investigated these two possibilities here by examining how the looking behavior of recipients affects pointing in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). Upon pointing to food, subjects were faced with a recipient who either looked at the indicated object (successful-look) or failed to look at the indicated object (failed-look). We predicted that, if apes point primarily to direct attention, subjects would spend more time pointing in the failed-look condition because the goal of their gesture had not been met. Alternatively, we expected that, if apes point primarily to request an object, subjects would not differ in their pointing behavior between the successful-look and failed-look conditions because these conditions differed only in the looking behavior of the recipient. We found that subjects did differ in their pointing behavior across the successful-look and failed-look conditions, but contrary to our prediction subjects spent more time pointing in the successful-look condition. These results suggest that apes are sensitive to the attentional states of gestural recipients, but their adjustments are aimed at multiple goals. We also found a greater number of individuals with a strong right-hand than left-hand preference for pointing.

Perception of facial expressions reveals selective affect-biased attention in humans and orangutans.

Rapid detection and recognition of another individual's emotional state plays a pivotal role for humans and, most likely, other social species. Proper reactions contribute to an individual's survival in potentially dangerous situations; this is ensured by a preferential attention towards salient cues. The predisposition to attend to certain categories of affectively salient stimuli- also referred to as affect-biased attention - is likely shared with other species, since fast detection of and appropriate reaction to threats is crucial to survival. We compared human children and one of our close relatives, Sumatran orangutans (Pongo abelii), and predicted that both look more attentively and longer at emotionally salient facial expressions of their own and corresponding other species, compared to neutral faces. However, in contrast to a bias towards emotions providing relevant information by indicating a threat, both species preferentially looked at the fear-related, but not the angry faces of humans and consistently preferred the silent-bared teeth espressions in orangutans. The differential attention towards certain expressions might derive from their social function and the need to detect a potential threat in the environment. Our findings are consistent with claims rooting this affect-biased attention characteristic of human perception in our evolutionary history.