The aim of the present study was twofold: First, we wanted to revisit the claim that human cooperative communication evolved as part of a larger, uniquely human, adaptation for cooperation and cultural life in general1,2. Second, we examined whether bonobos are the better model species for understanding the prerequisites of human communication10. To do so, we investigated whether bonobos and chimpanzees, both of which engage in general cooperative activities11,12,13, use distinct features characteristic of human social action in conversation16,17. By taking into consideration intra- and inter-species variability and by focusing on the mother-infant dyad, our results showed that all observed dyads across groups frequently engaged in turn-taking sequences to negotiate joint travel. They established participation frameworks via gaze, body orientation and the adjustment of initiation distance, and they used adjacency pair-like sequences characterized by gesture-response pairs and response waiting. Regarding temporal relationships between signals and responses, we found that mother-infant dyads of both species used the whole spectrum of responses, including immediate, overlapping and even delayed responses. Immediate responses match the temporal relations between turns in human speech consisting of relatively little cultural variation (e.g. overall cross-linguistic median of 100 ms, ranging from 0 ms in the English and Japanese culture, for instance, to 300 ms in the Danish and Lao culture)19. Our findings therefore support and expand the results of Rossano15, by demonstrating that gestural exchanges observed in mother-infant dyads of bonobos and chimpanzees are often very similar in timing to human action in conversation and embody the most crucial features of human cooperative conversation4,27: These gestural exchanges are bidirectional coordination devices, comprising the two implicit roles of signaller and recipient. In learning to use these gestures, individuals learn to play and to comprehend both roles no matter which role they are performing (soliciting to leave a location or being solicited to leave a location). Although we recently showed that chimpanzee mothers and their infants differ in many of the gesture types employed to initiate joint travel30, gestures shared by mothers and infants might involve role-reversal imitation (i.e. when one uses a gesture toward others the way others have used this gesture toward oneself), but also take the other’s perspectives on the event of joint travel. Furthermore, to reach the joint goal (of leaving a location), signallers made efforts to communicate in ways that were comprehensible to the recipient, for instance by combining initiatory behaviours with gaze and orienting the body to recipients. In addition, they seemed to ‘clarify’ the intended goal by using several adjacency pair-like sequences composed of the same or different gestures, when the first communicative attempt had not been successful. Turn-taking sequences of pre-linguistic human children go a step further in that recipients ask for clarification when needed and employ ‘negotiation of meaning’33. Furthermore, the rapid turn-taking in human conversation involves indefinite varying contents of turns, multi-modal deployment of vocal and gestural signals, and also seems without parallel, given the sheer amount of time and effort invested in communication31 (but see for nonhuman primates and birds34,35).

Overall, our findings strengthen a recent proposal by Levinson and Holler31 emphasizing the role of turn-taking behaviour for evolutionary scenarios of human language. They suggest that human language, despite its tight integration of speech and gesture, is a system composed of layers of abilities of different types and different antiquity. Thus, unpeeling the layers should enable us to understand the evolution of human language from an original rapid exchange of gestural or vocal material, into a system where the complexity of the linguistic and gestural material that is expressed in relatively short bursts has grown to the very limits that human cognition can process31.

In sum, sequentially organized, cooperative social interactions are not simply by-products of individuals living in human enculturated environments15, but play a crucial role in communicative exchanges of mother-infant dyads of bonobos and chimpanzees living under active selection pressures. These results challenge the human-ape divide, which suggests that human cooperative communication evolved as part of a larger adaptation of humans’ species-unique forms of cooperation2 ratcheted via existing and simpler components of primate cognition, such as group action and manipulative communication26. Our findings indicate that cooperative communicative interactions seem to play a crucial role in mother-infant dyads of bonobos and chimpanzees and, more generally, in nonhuman animals, for which shared goals and relatively low levels of competition prevail. Similarly to the universally organized social-interaction matrix of human conversation19, the results suggest that our closest living relatives have a strong universal infrastructure underlying their gestural interactions, which serves to minimize gaps and overlaps and allows for efficient information exchange. Further research on the methods and model species commonly used to draw inferences about evolutionary precursors to human communication is warranted (see for recent developments in other areas of cognitive ethology36), to enable (i) higher sensitivity to the social characteristics and/or ecology of a given species and (ii) a vital understanding of the structure and cognitive complexity underlying turn-taking sequences14 and communicative exchanges such as vocal alternations34 and duetting37.

Concerning our second aim of examining whether bonobos are the better models for precursors to human communication, a comparison of the investigated parameters showed behavioural differences between species, but not within species. Specifically, bonobo dyads (i) accompanied their signals more frequently with gaze, (ii) stayed in closer spatial proximity to each other for mother-infant coordination, and (iii) preferred to use overlapping and immediate responses. In contrast, chimpanzee dyads (i) were more likely to orient their bodies toward a recipient before signalling, (ii) showed a higher number of gesture-response pairs and response waiting, (iii) displayed overall more ‘communicative persistence’ to obtain the desired goal of joint travel, and (iv) used all three response tempi with relatively similar frequencies.

Three hypotheses may account for these observations. First, differences in communicative patterns may be explained by differences in ecological environments. For example, habitat characteristics such as thickness and growth of terrestrial herbaceous vegetation (THV) may differ considerately between the sites, resulting in different degrees of visibility and thus communication space and eye contact. Although THV is clearly more prevalent in bonobo habitats than in chimpanzee habitats38, differences in THV might also exist between the two chimpanzee habitats, resulting in relatively higher levels of visibility at Kanyawara38 compared to Taï South39. If this hypothesis were true, we would have expected to find differences in communicative behaviours between the Kanyawara and the Taï South community and between bonobos and chimpanzees in general. This does not accord with our observations.

Second, differences in communication styles between bonobos and chimpanzees are a by-product of the studied age range, particularly because chimpanzee infants may generally develop more quickly than do bonobo infants. For instance, Kuroda40 suggested that growth rates of bonobos and chimpanzees differ considerably, such that bonobos undergo a slower development of (i) spatial independence, (ii) locomotor skills (e.g. climbing, walking quadrupedally, riding on mother’s back), and (iii) social interactions with conspecifics (e.g. approaching, playing). This proposed delay in general development in bonobos may also have a crucial impact on the speed of communicatory skill development. If this hypothesis were true, we would have expected to find that age had a significant impact on the investigated parameters, with bonobo infants showing certain parameters such as use of gaze, adjustment of body orientation and response waiting, as well as overlapping responses, significantly later than chimpanzee infants. However, this was not the case. Body orientation and initiation distance were the only parameters for which a developmental effect was found, with increases of adjustment of body orientation towards mothers and initiation distance with age in both bonobo and chimpanzee infants. Overall, chimpanzee dyads initiated joint travel from larger distances than did bonobo dyads. These results are in line with findings of de Lathouwers and colleagues41, who showed that immature chimpanzees spend more time at larger distances from their mothers than do immature bonobos. Our study confirms that chimpanzees indeed develop spatial independence more quickly than do bonobos.

Third, bonobos and chimpanzees might employ different communication styles. Consistent with this hypothesis and based on our investigated parameters, bonobos and chimpanzees could be characterized by two clearly distinguishable communication styles accompanied by different temporal relationships: Bonobos frequently combined their communicative signals with gaze while in close proximity to the addressee, and they often used speedy responses. The underlying temporal relationships often matched those underlying human turn transition during speech19, with predominantly single adjacency pairs but also recipients responding before signals had been fully articulated. Chimpanzees, on the other hand, adjusted their body orientation toward recipients and used a generally slower mode of communication that involved more gesture-response pairs, higher frequencies of response waiting and delayed responses. Bonobo communication thus seems to resemble a subtle dance coined of flowing movements by signallers and recipients, while chimpanzee communication is structured with temporally separated and clearly recognizable units such as signal, pause and response. Chimpanzee signalling mirrors the structure of other social interactions, such as aggressive and grooming interactions, which are also characterized by typical negotiation sequences42,43, thereby demonstrating the significance of clearly structured interactions in chimpanzee society.

While future studies with additional age classes, communicative functions and dyads are of course mandatory, our study provides the first evidence that mother-infant dyads of bonobos and chimpanzees living in their natural environments employ different communication styles to convey the same message. Moreover, if certain communicative patterns are already observable in mother-infant coordination, the first step of co-regulated social interaction44, it is likely that these patterns are also crucial for general communication abilities of the species. Thus, generalization to behaviours of other dyads of a given community may be possible to some extent.

Although the long-standing bonobo-chimpanzee dichotomy has been challenged by new data emphasizing intra-species over inter-species variability28, bonobos and chimpanzees still seem to differ considerably concerning distinct characteristics of their social matrices. Males are more influential in chimpanzee society than in bonobo society45,46, with male chimpanzees heavily competing within their communities to gain indirect and direct fitness benefits13,46. This competition results in linear dominance hierarchies, male harassment and male-female dominance, but also strong social bonds and cooperative behaviour between males in the form of short- and long-term alliances (e.g. in the form of coalitionary behaviour, grooming, meat sharing and border patrols13,46). High levels of aggression, including lethal attacks, characterize intergroup encounters in chimpanzees, and infanticide has been observed within and between communities47. In contrast, bonobo society is characterized by co-dominance between the sexes, prolonged mother-son relationships45, and strong bonds between unrelated females45,48, resulting in a more flexible choice of coalition partners. Although between-group encounters in bonobos are usually friendly and peaceful49, there is anecdotal evidence of attempts of infanticide by males50 but also females51. Given the gregariousness of bonobo females, the threat of female infanticide could explain the need for close range communication between mothers and their dependant offspring.

It has been argued that species-specific social matrices and behaviours have been evolutionarily shaped by the distinctive morphology, connectivity and molecular biology of brain regions and pathways involved in social and environmental appraisal of threats and vigilance and control of emotional responses23,24. For instance, bonobos have more gray matter in the dorsal amygdala and a larger pathway linking the amygdala with the ventromedial prefrontal cortex (VMPFC)24. This neural circuitry has been implicated in both top-down control of aggressive impulses and bottom-up biases against harming others, as well as increased empathic sensitivity and prosocial behaviour24. In addition, bonobos have approximately twice the density of serotonergic axons in the amygdala compared to chimpanzees51, contributing to appraisal of the emotional context and significance of the environment52. These differences in neural circuitry are in line with recent experimental findings showing that bonobos tend to exhibit more cautious temperaments53, reduced ‘emotional reactivity’11, and greater tolerance when competing over food-resources36. The results of our study suggest that crucial features characterizing human communication, such as gaze and anticipation of recipients’ behaviour2,5, may be more significant in bonobo than in chimpanzee communication. Bonobos appear to exhibit a higher social awareness of the communicative situation and the anticipated meaning of a given signal, strengthening recent results demonstrating a bonobo-chimpanzee divergence in tasks requiring attention to social causality22.

Bonobos may therefore represent the most representative model for understanding the prerequisites of human communication10. However, additional analyses of the communicative and cognitive abilities of our closest living relatives are compulsory for a complete understanding of the impact of social and possibly cultural matrices on communication styles and tendencies. In addition, examples of convergent evolution in distantly related species can provide clues to the types of problems that particular communicative mechanisms are ‘designed’ to solve54,55. We thus hope to inspire future research that not only incorporates additional dyads and contexts, but also conducts taxonomically informed comparisons of species engaging in turn-taking behaviour during general interactions and communicative exchanges.

In sum, our results provide substantial evidence that the two primary model species for the origins of human behaviour, bonobos and chimpanzees, differ in their communication styles. While bonobos seem to anticipate and respond to signals before they have been fully articulated, chimpanzees engage in more time-consuming communicative negotiations. Both species use sequentially organized, cooperative social interactions to engage in a joint enterprise: Leaving together to another location. Their communicative interactions thus show the hallmarks of human social action during conversation and suggest that cooperative communication arose as a way of coordinating collaborative activities more efficiently. Our results strengthen a recent proposal by Levinson and Holler31 suggesting that the apparent gulf between animal and human communication may be bridged by looking for precursors adaptations to human language in turn-taking interactions.