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.

Who is calling? Optimizing source identification from marmoset vocalizations with hierarchical machine learning classifiers.

With their highly social nature and complex vocal communication system, marmosets are important models for comparative studies of vocal communication and, eventually, language evolution. However, our knowledge about marmoset vocalizations predominantly originates from playback studies or vocal interactions between dyads, and there is a need to move towards studying group-level communication dynamics. Efficient source identification from marmoset vocalizations is essential for this challenge, and machine learning algorithms (MLAs) can aid it. Here we built a pipeline capable of plentiful feature extraction, meaningful feature selection, and supervised classification of vocalizations of up to 18 marmosets. We optimized the classifier by building a hierarchical MLA that first learned to determine the sex of the source, narrowed down the possible source individuals based on their sex and then determined the source identity. We were able to correctly identify the source individual with high precisions (87.21%-94.42%, depending on call type, and up to 97.79% after the removal of twins from the dataset). We also examine the robustness of identification across varying sample sizes. Our pipeline is a promising tool not only for source identification from marmoset vocalizations but also for analysing vocalizations of other species.

Human Amygdala Volumetric Patterns Convergently Evolved in Cooperatively Breeding and Domesticated Species.

The amygdala is a hub in brain networks that supports social life and fear processing. Compared with other apes, humans have a relatively larger lateral nucleus of the amygdala, which is consistent with both the self-domestication and the cooperative breeding hypotheses of human evolution. Here, we take a comparative approach to the evolutionary origin of the relatively larger lateral amygdala nucleus in humans. We carry out phylogenetic analysis on a sample of 17 mammalian species for which we acquired single amygdala nuclei volumetric data. Our results indicate that there has been convergent evolution toward larger lateral amygdala nuclei in both domesticated and cooperatively breeding mammals. These results suggest that changes in processing fearful stimuli to reduce fear-induced aggression, which are necessary for domesticated and cooperatively breeding species alike, tap into the same neurobiological proximate mechanism. However, humans show changes not only in processing fearful stimuli but also in proactive prosociality. Since cooperative breeding, but not domestication, is also associated with increased proactive prosociality, a prominent role of the former during human evolution is more parsimonious, whereas self-domestication may have been involved as an additional stepping stone.

Is there a human fear paradox? A more thorough use of comparative data to test the fearful ape hypothesis.

Grossmann's intriguing proposal can benefit from a more thorough integration of the primate literature, particularly on neophobia. Moreover, it directly leads to strong predictions in callitrichids, the only other cooperatively breeding primates beyond humans, which may indeed be met: Being more likely to signal distress than independently breeding monkeys, and responding to such signals with approach and affiliation.

Putting the cart before the horse? The origin of information donation.

Heintz & Scott-Phillips propose that the partner choice ecology of our ancestors required Gricean cognitive pragmatics for reputation management, which caused a tendency toward showing and expecting prosociality that subsequently scaffolded language evolution. Here, we suggest a cognitively leaner explanation that is more consistent with comparative data and posits that prosociality and eventually language evolved along with cooperative breeding.

The evolutionary drivers of primate scleral coloration.

The drivers of divergent scleral morphologies in primates are currently unclear, though white sclerae are often assumed to underlie human hyper-cooperative behaviours. Humans are unusual in possessing depigmented sclerae whereas many other extant primates, including the closely-related chimpanzee, possess dark scleral pigment. Here, we use phylogenetic generalized least squares (PGLS) analyses with previously generated species-level scores of proactive prosociality, social tolerance (both n = 15 primate species), and conspecific lethal aggression (n = 108 primate species) to provide the first quantitative, comparative test of three existing hypotheses. The 'self-domestication' and 'cooperative eye' explanations predict white sclerae to be associated with cooperative, rather than competitive, environments. The 'gaze camouflage' hypothesis predicts that dark scleral pigment functions as gaze direction camouflage in competitive social environments. Notably, the experimental evidence that non-human primates draw social information from conspecific eye movements is unclear, with the latter two hypotheses having recently been challenged. Here, we show that white sclerae in primates are associated with increased cooperative behaviours whereas dark sclerae are associated with reduced cooperative behaviours and increased conspecific lethal violence. These results are consistent with all three hypotheses of scleral evolution, suggesting that primate scleral morphologies evolve in relation to variation in social environment.

Individual differences in co-representation in three monkey species (Callithrix jacchus, Sapajus apella and Macaca tonkeana) in the joint Simon task: the role of social factors and inhibitory control.

Behavioral coordination is involved in many forms of primate interactions. Co-representation is the simultaneous mental representation of one's own and the partner's task and actions. It often underlies behavioral coordination and cooperation success. In humans, the dyadic social context can modulate co-representation. Here, we first investigated whether individual differences in co-representation in the joint Simon task in capuchin monkeys and Tonkean macaques can be explained by social factors, namely dyadic grooming and sociality index, rank difference and eigenvector centrality. These factors did not predict variation in co-representation. However, in this specific task, co-representation reduces rather than facilitates joint performance. Automatic co-representation therefore needs to be inhibited or suppressed to maximize cooperation success. We therefore also investigated whether general inhibitory control (detour-reaching) would predict co-representation in the joint Simon task in Tonkean macaques, brown capuchin and marmoset monkeys. Inhibitory control did neither explain individual differences nor species differences, since marmosets were most successful in their joint performance despite scoring lowest on inhibitory control. These results suggest that the animals' ability to resolve conflicts between self and other representation to increase cooperation success in this task is gradually learned due to frequent exposure during shared infant care, rather than determined by strong general inhibitory control. Further, we conclude that the joint Simon task, while useful to detect co-representation non-invasively, is less suitable for identifying the factors explaining individual differences and thus a more fruitful approach to identify these factors is to design tasks in which co-representation favors, rather than hinders cooperation success.

Primate origins of corepresentation and cooperative flexibility: A comparative study with common marmosets (Callithrix jacchus), brown capuchins (Sapajus apella), and Tonkean macaques (Macaca tonkeana).

Human joint action is generally facilitated by the tendency to represent not only one's own task and behavior but also the partner's. Yet, under some conditions, such as in the joint Simon task, corepresentation can cause interference and hampers, rather than facilitates, joint performance. A competent cooperator should thus also be able to flexibly inhibit corepresentation if that is conducive to cooperation success. To investigate the evolutionary origin of corepresentation, as well as the cooperative flexibility to inhibit it when necessary, we tested brown capuchins and Tonkean macaques in the joint Simon task and compared them with the previously tested marmosets. Corepresentation was present in all 3 species, but its strength and the cooperation success varied substantially. The cooperatively breeding marmosets showed the weakest corepresentation effect and, therefore, highest cooperation success, and they were the only ones to use mutual gaze when coordination with the partner was necessary. Cooperative flexibility was therefore not correlated with brain size but with the prevalence of cooperation in nature. This conclusion was corroborated by species differences in gazing patterns and suggests that the drivers of cooperative flexibility in humans were not solely cognitive. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

After short interbirth intervals, captive callitrichine monkeys have higher infant mortality.

Life history theory predicts a trade-off between the quantity and quality of offspring. Short interbirth intervals-the time between successive births-may increase the quantity of offspring but harm offspring quality. In contrast, long interbirth intervals may bolster offspring quality while reducing overall reproductive output. Further research is needed to determine whether this relationship holds among primates, which have intensive parental investment. Using Cox proportional hazards models, we examined the effects of interbirth intervals (short, normal, or long) on infant survivorship using a large demographic dataset (n = 15,852) of captive callitrichine monkeys (marmosets, tamarins, and lion tamarins). In seven of the nine species studied, infants born after short interbirth intervals had significantly higher risks of mortality than infants born after longer interbirth intervals. These results suggest that reproduction in callitrichine primates may be limited by physiologic constraints, such that short birth spacing drives higher infant mortality.

Problem-solving in groups of common marmosets (Callithrix jacchus): more than the sum of its parts.

Human hypercooperativity and the emergence of division of labor enables us to solve problems not only effectively within a group but also collectively. Collective problem-solving occurs when groups perform better than the additive performance of separate individuals. Currently, it is unknown whether this is unique to humans. To investigate the evolutionary origin of collective problem-solving and potential precursors, we propose a continuum of group effects on problem-solving, from simple to complex ones, eventually culminating in collective problem-solving. We tested captive common marmosets with a series of problem-solving tasks, either alone or in a group. To test whether the performance of a group was more than the sum of its parts, we compared real groups to virtual groups (pooled scores of animals tested alone). Marmosets in real groups were both more likely to solve problems than marmosets within the virtual groups and to do so faster. Although individuals within real groups approached the problem faster, a reduction in neophobia was not sufficient to explain the greater success. Success within real groups arose because animals showed higher perseverance, especially after a fellow group member had found the solution in complex tasks. These results are consistent with the idea that group problem-solving evolved alongside a continuum, with performance improving beyond baseline as societies move from social tolerance to opportunities for diffusion of information to active exchange of information. We suggest that increasing interdependence and the adoption of cooperative breeding pushed our ancestors up this scale.

Monkey see, monkey feel? Marmoset reactions towards conspecifics' arousal.

Consolation has been observed in several species, including marmoset monkeys, but it is often unclear to what extent they are empathy-based. Marmosets perform well in at least two of three components of empathy-based consolation, namely understanding others and prosociality, but it is unknown to what extent they show matching with others. We, therefore, tested whether non-aroused individuals would become aroused themselves when encountering an aroused group member (indicated by piloerection of the tail). We found a robust contagion effect: group members were more likely to show piloerection themselves after having encountered an aroused versus relaxed conspecific. Moreover, group members offered consolation behaviours (affiliative approaches) towards the aroused fellow group members rather than the latter requesting it. Importantly, this pattern was shown by both aroused and non-aroused individuals, which suggests that they did not do this to reduce their own arousal but rather to console the individual in distress. We conclude that marmosets have all three components of empathy-based consolation. These results are in line with observations in another cooperative breeder, the prairie vole.

Reply to comment on "Nonadjacent dependency processing in monkeys, apes, and humans".

Rawski et al. revisit our recent findings suggesting the latent ability to process nonadjacent dependencies ("Non-ADs") in monkeys and apes. Specifically, the authors question the relevance of our findings for the evolution of human syntax. We argue that (i) these conclusions hinge upon an assumption that language processing is necessarily hierarchical, which remains an open question, and (ii) our goal was to probe the foundational cognitive mechanisms facilitating the processing of syntactic Non-ADs-namely, the ability to recognize predictive relationships in the input.

Intentional communication: solving methodological issues to assigning first-order intentional signalling.

Intentional signalling plays a fundamental role in human communication. Mapping the taxonomic distribution of comparable capacities may thus shed light on the selective pressures that enabled the evolution of human communication. Nonetheless, severe methodological issues undermine comparisons among studies, species and communicative modalities. Here, we discuss three main obstacles that hinder comparative research of 'first-order' intentional signalling (i.e. voluntary signalling in pursuit of a cognitively represented goal): (i) inconsistency in how behavioural hallmarks are defined and operationalised, (ii) testing of behavioural hallmarks without statistical comparison to control conditions, and (iii) bias against the publication of negative results. To address these obstacles, we present a four-step scheme with 20 statistical operational criteria to distinguish between non-intentional and first-order intentional signalling. Our unified scheme applies to visual and audible signals, thereby validating comparison across communicative modalities and species. This, in turn, promotes the generation and testing of hypotheses about the evolution of intentional communication.

Nonadjacent dependency processing in monkeys, apes, and humans.

The ability to track syntactic relationships between words, particularly over distances ("nonadjacent dependencies"), is a critical faculty underpinning human language, although its evolutionary origins remain poorly understood. While some monkey species are reported to process auditory nonadjacent dependencies, comparative data from apes are missing, complicating inferences regarding shared ancestry. Here, we examined nonadjacent dependency processing in common marmosets, chimpanzees, and humans using "artificial grammars": strings of arbitrary acoustic stimuli composed of adjacent (nonhumans) or nonadjacent (all species) dependencies. Individuals from each species (i) generalized the grammars to novel stimuli and (ii) detected grammatical violations, indicating that they processed the dependencies between constituent elements. Furthermore, there was no difference between marmosets and chimpanzees in their sensitivity to nonadjacent dependencies. These notable similarities between monkeys, apes, and humans indicate that nonadjacent dependency processing, a crucial cognitive facilitator of language, is an ancestral trait that evolved at least ~40 million years before language itself.

Validity of Cognitive Tests for Non-human Animals: Pitfalls and Prospects.

Comparative psychology assesses cognitive abilities and capacities of non-human animals and humans. Based on performance differences and similarities in various species in cognitive tests, it is inferred how their minds work and reconstructed how cognition might have evolved. Critically, such species comparisons are only valid and meaningful if the tasks truly capture individual and inter-specific variation in cognitive abilities rather than contextual variables that might affect task performance. Unlike in human test psychology, however, cognitive tasks for non-human primates (and most other animals) have been rarely evaluated regarding their measurement validity. We review recent studies that address how non-cognitive factors affect performance in a set of commonly used cognitive tasks, and if cognitive tests truly measure individual variation in cognitive abilities. We find that individual differences in emotional and motivational factors primarily affect performance via attention. Hence, it is crucial to systematically control for attention during cognitive tasks to obtain valid and reliable results. Aspects of test design, however, can also have a substantial effect on cognitive performance. We conclude that non-cognitive factors are a minor source of measurement error if acknowledged and properly controlled for. It is essential, however, to validate and eventually re-design several primate cognition tasks in order to ascertain that they capture the cognitive abilities they were designed to measure. This will provide a more solid base for future cognitive comparisons within primates but also across a wider range of non-human animal species.

The emergence of emotionally modern humans: implications for language and learning.

According to the Cooperative Breeding Hypothesis, apes with the life-history attributes of those in the line leading to the genus Homo could not have evolved unless male and female allomothers had begun to help mothers care for and provision offspring. As proposed elsewhere, the unusual way hominins reared their young generated novel phenotypes subsequently subjected to Darwinian social selection favouring those young apes best at monitoring the intentions, mental states and preferences of others and most motivated to attract and appeal to caretakers. Not only were youngsters acquiring information in social contexts different from those of other apes, but they would also have been emotionally and neurophysiologically different from them in ways that are relevant to how humans learn. Contingently delivered rewards to dependents who attracted and ingratiated themselves with allomothers shaped their behaviours and vocalizations and transformed the way developing youngsters learned from others and internalized their preferences. This article is part of the theme issue 'Life history and learning: how childhood, caregiving and old age shape cognition and culture in humans and other animals'.

Marmoset prosociality is intentional.

Marmoset monkeys show high levels of proactive prosociality, a trait shared with humans, presumably because both species rely on allomaternal care. However, it is not clear whether the proximate regulation of this convergent trait is also similar, in particular with regard to intentionality, which is a defining characteristic of prosocial behavior in the human literature. The aim of this paper was to investigate whether marmoset monkeys' prosociality fulfils the criteria of intentionality developed in primate communication research. The results show that marmoset prosocial behavior (i) has some degree of flexibility, since individuals can use multiple means to reach their goal and adjust them to specific conditions, (ii) depends on the presence of an audience, i.e. potential recipients (social use), and (iii) is goal-directed, because (a) it continues exactly until the putative goal is reached, and (b) individuals check back and look at/for their partner when their prosocial actions do not achieve the putative goal (i.e. if their actions don't lead to the expected outcome, this elicits distinct reactions in the actor). These results suggest that marmoset prosociality is under some degree of voluntary, intentional control. They are in line with other findings that marmosets perceive each other as intentional agents, and only learn socially from actions that are perceived as intentional. The most parsimonious conclusion is, therefore, that prosocial behavior is fundamentally under voluntary control in marmosets, just as it is in humans, even though our more sophisticated cognitive abilities allow for a far more complex integration of prosociality into a broader variety of contexts and of behavioral goals.

Are dialects socially learned in marmoset monkeys? Evidence from translocation experiments.

The acoustic properties of vocalizations in common marmosets differ between populations. These differences may be the result of social vocal learning, but they can also result from environmental or genetic differences between populations. We performed translocation experiments to separately quantify the influence of a change in the physical environment (experiment 1), and a change in the social environment (experiment 2) on the acoustic properties of calls from individual captive common marmosets. If population differences were due to genetic differences, we expected no change in the vocalizations of the translocated marmosets. If differences were due to environmental factors, we expected vocalizations to permanently change contingent with environmental changes. If social learning was involved, we expected that the vocalizations of animals translocated to a new population with a different dialect would become more similar to the new population. In experiment 1, we translocated marmosets to a different physical environment without changing the social composition of the groups or their neighbours. Immediately after the translocation to the new facility, one out of three call types showed a significant change in call structure, but 5-6 weeks later, the calls were no longer different from before the translocation. Thus, the novel physical environment did not induce long lasting changes in the vocalizations of the marmosets. In experiment 2, we translocated marmosets to a new population with a different dialect. Importantly, our previous work had shown that these two populations differed significantly in vocalization structure. The translocated marmosets were still housed in their original social group, but after translocation they were surrounded by the vocalizations from neighbouring groups of the new population. The vocal distance between the translocated individuals and the new population decreased for two out of three call types over 16 weeks. Thus, even without direct social contact or interaction, the vocalizations of the translocated animals converged towards the new population, indicating that common marmosets can modify their calls due to acoustic input from conspecifics alone, via crowd vocal learning. To our knowledge, this is the first study able to distinguish between different explanations for vocal dialects as well as to show crowd vocal learning in a primate species.

A comparative study of litter size and sex composition in a large dataset of callitrichine monkeys.

In many birds and mammals, the size and sex composition of litters can have important downstream effects for individual offspring. Primates are model organisms for questions of cooperation and conflict, but the factors shaping interactions among same-age siblings have been less-studied in primates because most species bear single young. However, callitrichines (marmosets, tamarins, and lion tamarins) frequently bear litters of two or more, thereby providing the opportunity to ask whether variation in the size and sex composition of litters affects development, survival, and reproduction. To investigate these questions, we compiled a large dataset of nine species of callitrichines (n = 27,080 individuals; Callithrix geoffroyi, Callithrix jacchus, Cebuella pygmaea, Saguinus imperator, Saguinus oedipus, Leontopithecus chrysomelas, Leontopithecus chrysopygus, Leontopithecus rosalia, and Callimico goeldii) from zoo and laboratory populations spanning 80 years (1938-2018). Through this comparative approach, we found several lines of evidence that litter size and sex composition may impact fitness. Singletons have higher survivorship than litter-born peers and they significantly outperform litter-born individuals on two measures of reproductive performance. Further, for some species, individuals born in a mixed-sex litter outperform isosexually-born individuals (i.e., those born in all-male or all-female litters), suggesting that same-sex competition may limit reproductive performance. We also document several interesting demographic trends. All but one species (C. pygmaea) has a male-biased birth sex ratio with higher survivorship from birth to sexual maturity among females (although this was significant in only two species). Isosexual litters occurred at the expected frequency (with one exception: C. pygmaea), unlike other animals, where isosexual litters are typically overrepresented. Taken together, our results indicate a modest negative effect of same-age sibling competition on reproductive output in captive callitrichines. This study also serves to illustrate the value of zoo and laboratory records for biological inquiry.

Food sharing patterns in three species of callitrichid monkeys (Callithrix jacchus, Leontopithecus chrysomelas, Saguinus midas): Individual and species differences.

Food sharing (FS) in cooperatively breeding callitrichids is unusual among nonhuman primates because they regularly share significant amounts of preferred food with immatures and engage in proactive FS. However, it is still unclear which classes of individuals (males or females, breeders or helpers) engage most in FS, and whether differences exist among callitrichid species. In the first part of this study, we characterized general FS patterns in common marmosets (Callithrix jacchus). We found substantial adult-immature FS, and female breeders shared the least with immatures. This conflicts with previously published studies, where data were collected with the prevailing standard method of providing a food bowl to the entire group. In the second part, a comparison of our access-bias-free method and the standard method suggested that previous findings are likely the result of access bias. In the third part, we investigated species differences in adult-adult FS among common marmosets, golden-headed lion tamarins (Leontopithecus chrysomelas), and red-handed tamarins (Saguinus midas). As common marmosets show lower levels of interdependence within groups, we expected more adult-adult FS in tamarins compared with marmosets. Adult-adult FS was indeed more prevalent in tamarins and not exclusively directed from male breeders to female breeders. Therefore, our results suggest that adult-adult FS in marmosets mostly reflects the high energetic demands of female breeders, whereas in the more interdependent tamarins, it may be used to reinforce cooperative bonds between adult group members. (PsycINFO Database Record (c) 2019 APA, all rights reserved).