Proactive, that is, unsolicited, prosociality is a key component of our hyper-cooperation, which in turn has enabled the emergence of various uniquely human traits, including complex cognition, ...morality and cumulative culture and technology. However, the evolutionary foundation of the human prosocial sentiment remains poorly understood, largely because primate data from numerous, often incommensurable testing paradigms do not provide an adequate basis for formal tests of the various functional hypotheses. We therefore present the results of standardized prosociality experiments in 24 groups of 15 primate species, including humans. Extensive allomaternal care is by far the best predictor of interspecific variation in proactive prosociality. Proactive prosocial motivations therefore systematically arise whenever selection favours the evolution of cooperative breeding. Because the human data fit this general primate pattern, the adoption of cooperative breeding by our hominin ancestors also provides the most parsimonious explanation for the origin of human hyper-cooperation.
Abstract
Recent studies find increasing evidence for vocal accommodation in nonhuman primates, indicating that this form of vocal learning is more prevalent than previously thought. Convergent vocal ...accommodation (i.e. becoming more similar to partners) indicates social closeness. At the same time, however, becoming too similar may compromise individual recognisability. This is especially problematic if individual recognisability is an important part of the call function, like in long-distance contact calls. In contrast, in calls with a different function, the trade-off between signalling social closeness and individual recognisability might be less severe. We therefore hypothesized that the extent and consequences of accommodation depend on the function of a given call, and expected (1) more accommodation in calls for which individual identity is less crucial and (2) that individual identity is less compromised in calls that serve mainly to transmit identity compared to calls where individual recognisability is less important. We quantified vocal accommodation in three call types over the process of pair formation in common marmoset monkeys (
Callithrix jacchus
,
n
= 20). These three call types have different functions and vary with the degree to which they refer to individual identity of the caller. In accordance with our predictions, we found that animals converged most in close contact calls (trill calls), but less in calls where individual identity is more essential (phee- and food calls). In two out of three call types, the amount of accommodation was predicted by the initial vocal distance. Moreover, accommodation led to a drop in statistical individual recognisability in trill calls, but not in phee calls and food calls. Overall, our study shows that patterns of vocal accommodation vary between call types with different functions, suggestive of trade-offs between signalling social closeness and individual recognisability in marmoset vocalizations.
Joint action has increasingly become a key topic to understand the emergence of the human mind. The phenomenon is closely linked to several theoretical concepts, such as shared intentionality, which ...are difficult to operationalize empirically. We therefore employ a paradigm-driven, bottom-up approach, and as such discuss co-representing the partner’s and one’s own actions as key mechanism for joint action. After embedding co-representation in the broader landscape of related theoretical concepts, we review neurobiological, ontogenetic, and phylogenetic studies, with a focus on whether co-representation and its flexible deployment should be construed as a low- or high-level cognitive process. The empirical findings convergently suggest that co-representation does not require strong inhibitory skills or mentalistic understanding and occurs automatically. Moreover, more cooperative species are better at flexibly suppressing co-representation when required for cooperation success, and frequently rely on cooperation markers, such as mutual gaze. We thus contribute to closing the current gap between theoretical concepts related to joint action research and their empirical investigation, and end by highlighting additional approaches for doing so.
•Joint action plays a key role for the ontogeny and evolution of the human mind.•We examine co-representation (CR) as key mechanism for joint action.•Our paradigm-driven review integrates evidence on CR from diverse disciplines and species.•Cooperative species flexibly employ CR and use mutual gaze to aid coordination.•Empirical research on joint action needs universal operationalization criteria.
Despite sharing a recent common ancestor, humans are surprisingly different from other great apes. The most obvious discontinuities are related to our cognitive abilities, including language, but we ...also have a markedly different, cooperative breeding system. Among many nonhuman primates and mammals in general, cooperative breeding is accompanied by psychological changes leading to greater prosociality, which directly enhances performance in social cognition. Here we propose that these cognitive consequences of cooperative breeding could have become more pervasive in the human lineage because the psychological changes were added to an ape‐level cognitive system capable of understanding simple mental states, albeit mainly in competitive contexts. Once more prosocial motivations were added, these cognitive abilities could also be used for cooperative purposes, including a willingness to share mental states, thereby enabling the emergence of shared intentionality. Shared intentionality has been identified as the original source of many uniquely human cognitive abilities, including cumulative culture and language. Shared intentionality rests on a fundamentally prosocial disposition that is strikingly absent in chimpanzees, but present in cooperatively breeding primates. Thus, our hypothesis is that while chimpanzees and perhaps all great apes exhibit many of the important cognitive preconditions for uniquely human mental capacities to evolve, they lack the psychological preconditions. In humans, we argue, the two components merged, the cognitive component due to common descent from ape ancestors and the motivational component due to convergent evolution of traits typical of many cooperative breeders.
Measuring body surface temperature changes with infrared thermography has recently been put forward as a non-invasive alternative measure of physiological correlates of emotional reactions. In ...particular, the nasal region seems to be highly sensitive to emotional reactions. Several studies suggest that nasal temperature is negatively correlated with the level of arousal in humans and other primates, but some studies provide inconsistent results. Our goal was to establish the use of infrared thermography to quantify emotional reactions in common marmosets (Callithrix jacchus), with a focus on the nasal region. To do so we exposed 17 common marmosets to a set of positive, negative and control stimuli (positive: preferred food, playback of food calls; negative: playback of aggressive vocalizations, teasing; control: no stimulus). We compared nasal temperature before and after the stimuli and expected that highly aroused emotional states would lead to a drop in nasal temperature. To validate the thermography measure, we coded piloerection of the tail as an independent measure of arousal and expected a negative correlation between the two measures. Finally, we coded physical activity to exclude its potential confounding impact on nasal temperature. Our results show that all predictions were met: the animals showed a strong decrease in nasal temperature after the presentation of negative arousing stimuli (teasing, playback of aggressive vocalizations). Furthermore, these changes in nasal temperature were correlated with piloerection of the tail and could not be explained by changes in physical activity. In the positive and the control conditions, we found systematic sex differences: in males, the preferred food, the playbacks of food calls, as well as the control stimulus led to an increase in nasal temperature, whereas in females the temperature remained stable (preferred food, control) or decreased (playback of food calls). Based on naturalistic observations that document higher food motivation and competition among female marmosets, as well as stronger reactions to separation from group members in male marmosets, these sex differences corroborate a negative correlation between arousal and nasal temperature. Overall, our results support that measuring nasal temperature by infrared thermography is a promising method to quantify emotional arousal in common marmosets in a fully non-invasive and highly objective way.
•We investigated the use of infrared thermography to study emotional states in common marmosets.•Nasal temperature dropped in response to negative stimuli in males and females.•Nasal temperature drops as a measure of arousal was validated by a behavioral measure of arousal (piloerection) and was not an artefact of activity.•The thermal reaction in the positive and the control conditions varied between males and females, consistent with known sex differences in food motivation.•Nasal temperature changes are a more sensitive measure of arousal than piloerection.
To understand the primate origins of the human interaction engine, it is worthwhile to focus not only on great apes but also on callitrichid monkeys (marmosets and tamarins). Like humans, but unlike ...great apes, callitrichids are cooperative breeders, and thus habitually engage in coordinated joint actions, for instance when an infant is handed over from one group member to another. We first explore the hypothesis that these habitual cooperative interactions, the marmoset interactional ethology, are supported by the same key elements as found in the human interaction engine: mutual gaze (during joint action), turn-taking, volubility, as well as group-wide prosociality and trust. Marmosets show clear evidence of these features. We next examine the prediction that, if such an interaction engine can indeed give rise to more flexible communication, callitrichids may also possess elaborate communicative skills. A review of marmoset vocal communication confirms unusual abilities in these small primates: high volubility and large vocal repertoires, vocal learning and babbling in immatures, and voluntary usage and control. We end by discussing how the adoption of cooperative breeding during human evolution may have catalysed language evolution by adding these convergent consequences to the great ape-like cognitive system of our hominin ancestors.
This article is part of the theme issue ‘Revisiting the human ‘interaction engine’: comparative approaches to social action coordination’.
Thornton & McAuliffe (2015) recently questioned the hypothesis that cooperative breeding has a variety of socio‐cognitive consequences, invoking both logical and empirical arguments. The cooperative ...breeding hypothesis (CBH) posits that the immediate tasks associated with extensive allomaternal care require motivational proximate mechanisms, such as increased social tolerance or proactive prosociality which, as a side‐effect, also can facilitate performance in socio‐cognitive tasks. Eventually, over evolutionary time this constellation may also, under specific conditions, facilitate increases in brain size. Thus, the CBH is not merely a modified version of the social brain hypothesis, as suggested by Thornton & McAuliffe, which would posit that a species has to be particularly smart to engage in cooperative breeding. In this reply, we first clarify these conceptual issues and then systematically address their criticism of the empirical evidence. We conclude that the empirical evidence for the CBH is strong in primates, but that future work on lineages other than primates is required to assess its generality.
Thornton & McAuliffe (2015) recently questioned the cooperative breeding hypothesis (CBH), i.e. that cooperative breeding has a variety of socio‐cognitive consequences. However, the CBH is not merely a modified version of the social brain hypothesis as implied by Thornton & McAuliffe, since it does not claim that a species would have to be particularly smart to engage in cooperative breeding. Rather, the CBH posits that the immediate tasks associated with extensive allomaternal care require motivational proximate mechanisms, such as increased social tolerance and proactive prosociality, which, as a side effect also can facilitate performance in socio‐cognitive tasks. Eventually, over evolutionary times this constellation may also, under specific conditions, facilitate increases in brain size. We first clarify these conceptual issues and then address the criticism of the empirical evidence. We conclude that the evidence for the CBH is strong for primates, and future work on other lineages will reveal its generality.
The Global Deal for Nature (GDN) is a time-bound, science-driven plan to save the diversity and abundance of life on Earth. Pairing the GDN and the Paris Climate Agreement would avoid catastrophic ...climate change, conserve species, and secure essential ecosystem services. New findings give urgency to this union: Less than half of the terrestrial realm is intact, yet conserving all native ecosystems-coupled with energy transition measures-will be required to remain below a 1.5°C rise in average global temperature. The GDN targets 30% of Earth to be formally protected and an additional 20% designated as climate stabilization areas, by 2030, to stay below 1.5°C. We highlight the 67% of terrestrial ecoregions that can meet 30% protection, thereby reducing extinction threats and carbon emissions from natural reservoirs. Freshwater and marine targets included here extend the GDN to all realms and provide a pathway to ensuring a more livable biosphere.
For small, arboreal marmoset monkeys, antipredator vigilance is essential to ensure survival. However, since antipredator vigilance is incompatible with some other behaviours, such as feeding in a ...head-down position, it has to be regulated efficiently within individuals and perhaps even at the group level. To investigate what drives individual differences in vigilance and feeding behaviour in common marmosets, Callithrix jacchus, and whether they adjust these behaviours to each other, we collected behavioural data on 14 marmosets in contexts where feeding and vigilance were mutually exclusive. The presence of infants resulted in higher overall vigilance and less feeding. Moreover, individuals increased their vigilance when the pair mate was feeding and thus could not be vigilant itself. They thus adjusted their own vigilance to the risk level of their pair mate, which resulted in a turn taking-like pattern of feeding and being vigilant in the pair. This flexibility of vigilance is consistent with marmosets' sensitivity to other's needs in another context, food sharing, when sharing is increased when food is more difficult to obtain. Together, these results suggest considerable awareness of the current state of group members in common marmosets.
•Marmosets increased their vigilance when the partner was feeding head down.•This resulted in a turn-taking-like pattern of feeding and being vigilant.•Adults increased their vigilance and decreased feeding when infants were present.•Marmoset vigilance is flexible and takes others' risk level into account.