Communicative roots of complex sociality and cognition: preface to the theme issue.

Primates live in stable social groups in which they form differentiated relationships with group members and use a range of communication including facial expressions, vocalizations and gestures. However, how these different types of communication are used to regulate social interactions, and what cognitive skills underpin this communication, is still unclear. The aim of this special issue is to examine the types of cognitive skills underpinning the flexible and complex communication that is used to maintain the bonded social relationships found in primates and humans. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Communicative roots of complex sociality and cognition: neuropsychological mechanisms underpinning the processing of social information.

Primate social bonds are described as being especially complex in their nature, and primates have unusually large brains for their body size compared to other mammals. Communication in primates has attracted considerable attention because of the important role it plays in social bonding. It has been proposed that differentiated social relationships are cognitively complex because primates need to continuously update their knowledge about different types of social bonds. Therefore, primates infer whether an opportunity for social interaction is rewarding (valuable to individual goals) based on their knowledge of the social relationships of the interactants. However, exposure to distraction and stress has detrimental effects on the dopaminergic system, suggesting that understanding social relationships as rewarding is affected in these conditions. This paper proposes that complex communication evolved to augment the capacity to form social relationships during stress through flexibly modifying intentionality in communication (audience checking, response waiting and elaboration). Intentional communication may upregulate dopamine dynamics to allow recognition that an interaction is rewarding during stress. By examining these associations between complexity of communication and stress, we provide new insights into the cognitive skills involved in forming social bonds in primates and the evolution of communication systems in both primates and humans. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Communicative roots of complex sociality and cognition.

Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non-human primates and humans. To move the field forward and carry out both within- and among-species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.

Social and ecological complexity is associated with gestural repertoire size of wild chimpanzees.

Increasing our understanding of primate gestural communication can provide new insights into language evolution. A key question in primate communication is the association between the social relationships of primates and their repertoire of gestures. Such analyses can reveal how primates use their repertoire of gestural communication to maintain their networks of family and friends, much as humans use language to maintain their social networks. In this study we examined the association between the repertoire of gestures (overall, manual and bodily gestures, and gestures of different modalities) and social bonds (presence of reciprocated grooming), coordinated behaviors (travel, resting, co-feeding), and the complexity of ecology (e.g. noise, illumination) and sociality (party size, audience), in wild East African chimpanzees (Pan troglodytes schweinfurthii). A larger repertoire size of manual, visual gestures was associated with the presence of a relationship based on reciprocated grooming and increases in social complexity. A smaller repertoire of manual tactile gestures occurred when the relationship was based on reciprocated grooming. A smaller repertoire of bodily gestures occurred between partners who jointly traveled for longer. Whereas gesture repertoire size was associated with social complexity, complex ecology also influenced repertoire size. The evolution of a large repertoire of manual, visual gestures may have been a key factor that enabled larger social groups to emerge during evolution. Thus, the evolution of the larger brains in hominins may have co-occurred with an increase in the cognitive complexity underpinning gestural communication and this, in turn, may have enabled hominins to live in more complex social groups.

Gestural repertoire size is associated with social proximity measures in wild chimpanzees.

Studying the communication systems of primates can provide insights into the evolutionary origins of human language. Some theories propose that language evolved to help meet the demands of managing complex social relationships. Examining the associations between sociality and communication in the great apes can help to identify the specific selection pressures that may have been important for language evolution. In particular, gestural communication is believed to be important because it is a relatively recent trait seen only in primates and particularly in the great apes. However, the extent to which more complex gestural communication plays a role in managing social relationships, as compared to less complex gestural communication, is not well understood. Using social network analysis, we examined the association between complex gesturing (indexed as repertoire size) and complexity of social relationships indexed as proximity (the duration of time spent within 10 m, per hour spent in same party) in wild chimpanzees (Pan troglodytes schweinfurthii). Repertoire size (the total number of gesture types a focal subject produced toward other individuals) and dyadic repertoire size (the number of gesture types produced toward the dyad partner, per hour spent within 10 meters) were positively associated with proximity at the level of the group (centrality in the proximity network) and the dyad (proximity duration between dyads), respectively. Further, the repertoire size of visual and auditory short-range gestures was positively associated with proximity, while the repertoire size of tactile gesture was negatively associated with proximity. Overall these results suggest that gestural repertoire size has important implications for maintaining social relationships in wild chimpanzees and more broadly that gestural communication may have played an important role in language evolution.

Social Brain Hypothesis: Vocal and Gesture Networks of Wild Chimpanzees.

A key driver of brain evolution in primates and humans is the cognitive demands arising from managing social relationships. In primates, grooming plays a key role in maintaining these relationships, but the time that can be devoted to grooming is inherently limited. Communication may act as an additional, more time-efficient bonding mechanism to grooming, but how patterns of communication are related to patterns of sociality is still poorly understood. We used social network analysis to examine the associations between close proximity (duration of time spent within 10 m per hour spent in the same party), grooming, vocal communication, and gestural communication (duration of time and frequency of behavior per hour spent within 10 m) in wild chimpanzees. This study examined hypotheses formulated a priori and the results were not corrected for multiple testing. Chimpanzees had differentiated social relationships, with focal chimpanzees maintaining some level of proximity to almost all group members, but directing gestures at and grooming with a smaller number of preferred social partners. Pairs of chimpanzees that had high levels of close proximity had higher rates of grooming. Importantly, higher rates of gestural communication were also positively associated with levels of proximity, and specifically gestures associated with affiliation (greeting, gesture to mutually groom) were related to proximity. Synchronized low-intensity pant-hoots were also positively related to proximity in pairs of chimpanzees. Further, there were differences in the size of individual chimpanzees' proximity networks-the number of social relationships they maintained with others. Focal chimpanzees with larger proximity networks had a higher rate of both synchronized low- intensity pant-hoots and synchronized high-intensity pant-hoots. These results suggest that in addition to grooming, both gestures and synchronized vocalizations may play key roles in allowing chimpanzees to manage a large and differentiated set of social relationships. Gestures may be important in reducing the aggression arising from being in close proximity to others, allowing for proximity to be maintained for longer and facilitating grooming. Vocalizations may allow chimpanzees to communicate with a larger number of recipients than gestures and the synchronized nature of the pant-hoot calls may facilitate social bonding of more numerous social relationships. As group sizes increased through human evolution, both gestures and synchronized vocalizations may have played important roles in bonding social relationships in a more time-efficient manner than grooming.