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Marmoset monkeys overcome dyadic social dilemmas while avoiding mutual defection
Abstract
Social primates constantly face situations in which their preferences collide and they need to engineer strategies to overcome conflicts of interest. Studies with chimpanzees, Pan troglodytes, have found that they use competitive strategies to overcome social dilemmas, maximizing their own benefits while minimizing the loss of rewards. However, little is known about how other primates that rely more on cooperation would overcome similar dilemmas. We therefore presented male–female pairs of common marmosets, Callithrix jacchus (cooperative breeders) with two experiments of an action-based paradigm that creates a conflict of interest over access to an unequal reward distribution. Rather than engaging in mutual defection, marmosets were able to overcome this social dilemma over time, by developing a mix of strategic behaviours (predominantly by females) and tolerance to disadvantageous reward distributions (predominantly by males). This mix of behavioural strategies yielded more and better rewards for the females. Importantly, such a net outcome is consistent with the natural history of this species where females, who carry a high energetic burden of reproduction, tend to be less prosocial and are receivers, rather than donors, in food-sharing events among adults.
... Squirrel monkeys were able to coordinate with their partner to obtain the highest rewards. In another recent study, Sánchez-Amaro and colleagues 18 presented for the first time pairs of common marmosets (Callithrix jacchus) with a social dilemma modeled after the snowdrift game 10,19 . In this study, marmosets could access an unequal reward distribution in the form of a rotating tray. ...
... Thus, the second possible explanation for our results is that gibbons interpreted the situation as a conflict of interest and hesitated to pull to avoid losing rewards in favor of the passive partner. This interpretation would be in line with previous findings in chimpanzees, bonobos and common marmosets 10,16,18 . Thus, given the two nonmutually exclusive explanations, it remains unclear whether gibbons defected in indirect food test trials due to a reduced motivation to act because they could not access the extra reward attached to the handle (but still could benefit from the five rewards) or because they wanted to avoid the possibility of losing rewards to their partner. ...
Social primates face conflicts of interest with other partners when their individual and collective interests collide. Despite living in small, primarily bonded, groups compared to other social primates, gibbons are not exempt from these conflicts in their everyday lives. In the current task, we asked whether dyads of gibbons would solve a conflict of interest over food rewards. We presented dyads of gibbons with a situation in which they could decide whether to take an active role and pull a handle to release food rewards at a distance or take a passive role and avoid action. In this situation, the passive partner could take an advantageous position to obtain the rewards over the active partner. Gibbons participated in three conditions: a control condition with no food rewards, a test condition with indirect food rewards and a test condition with direct food rewards. In both test conditions, five rewards were released at a distance from the handle. In addition, the active individual could obtain one extra food reward from the handle in the direct food condition. We found that gibbons acted more often in the two conditions involving food rewards, and waited longer in the indirect compared to the direct food condition, thus suggesting that they understood the task contingencies. Surprisingly, we found that in a majority of dyads, individuals in the active role obtained most of the payoff compared to individuals in the passive role in both food conditions. Furthermore, in some occasions individuals in the active role did not approach the location where the food was released. These results suggest that while gibbons may strategize to maximize benefits in a competitive food task, they often allowed their partners to obtain better rewards. Our results highlight the importance of social tolerance and motivation as drivers promoting cooperation in these species.
... Barnacle geese pairs, for example, collectively defend preferred foraging sites within colonies; males stand guard during foraging, allowing females to eat more, and males defend eggs while females take incubation breaks (16). Zebra finches negotiate incubation using vocal duets (17), and bonded pairs of marmosets facing novel social dilemmas overcame them by developing new forms of cooperation (18). All of these activities entail effort and attention between partners. ...
Coordinated pair bonds are common in birds and also occur in many other taxa. How do animals solve the social dilemmas they face in coordinating with a partner? We developed an evolutionary model to explore this question, based on observations that a) neuroendocrine feedback provides emotional bookkeeping which is thought to play a key role in vertebrate social bonds and b) these bonds are developed and maintained via courtship interactions that include low-stakes social dilemmas. Using agent-based simulation, we found that emotional bookkeeping and courtship sustained cooperation in the iterated prisoner’s dilemma in noisy environments, especially when combined. However, when deceitful defection was possible at low cost, courtship often increased cooperation, whereas emotional bookkeeping decreased it.
Social dilemmas play an important role in the study of cooperative behaviours. In this experiment we tested the strategies adopted by tufted capuchin monkeys, Sapajus spp., when faced with a cooperative situation involving a conflict of interest, simulating a Snowdrift game. We tested 12 capuchin monkeys (six dyads) in two experimental conditions: Snowdrift (cooperation) and Competition. Monkeys had the opportunity to pull a string to move a rotating bar and obtain a reward while delivering a different reward to their partner. Pulling in the Snowdrift condition delivered a smaller reward to the individual pulling the string and a larger reward to the partner, while the opposite happened in the Competition condition. If neither monkey pulled within 30 s, neither received a reward. Monkeys were also individually tested in a battery of self-control tasks. Capuchin monkeys successfully coordinated (i.e. obtained a reward) in 100% of trials and flexibly adapted their behaviour to the different experimental conditions, by pulling earlier in the Competition and later in the Snowdrift condition. Dominance rank and self-control had no effect on the latencies to pull in either experimental condition. No evidence of any alternation strategy was observed. Our results suggest that capuchin monkeys can solve a conflict of interest without engaging in complex calculations.
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.
The decoy effect is a violation of rationality that occurs when the relative preference between two target options changes with the addition of a third option, called the decoy, that is no better than the target options but worse than one of the options on one attribute. The presence of the decoy increases the chance that the option that dominates it on this attribute is chosen over the other target option. The current study tested decoy effects with great apes' food preferences. We presented apes with two target items, grape and banana, and a third item, the decoy, which was either a smaller grape or a smaller piece of banana. We found that apes' decisions were not influenced by the presence of a decoy. In general, apes did not increase their choices in favor of the target item that dominated the decoy. This would indicate that great apes are not vulnerable to the cognitive biases that cause decoy effects in humans, at least in cases where choice is between two different types of food. We discuss what can be concluded about the psychological causes of human irrational choices and their evolutionary origin.
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.
Games from experimental economics have provided insights into the evolutionary roots of social decision making in primates and other species. Multiple primate species' abilities to cooperate, coordinate and anti-coordinate have been tested utilizing variants of these simple games. Past research, however, has focused on species known to cooperate and coordinate in the wild. To begin to address the degree to which cooperation and coordination may be a general ability that manifests in specific contexts, the present study assessed the decisions of squirrel monkeys (Saimiri boliviensis; N = 10), a species not known for their cooperative behavior in these games. Pairs of monkeys were presented with the Assurance Game (a coordination game), the Hawk-Dove Game (an anti-coordination game) and the Prisoner's Dilemma (a cooperation game with a temptation to defect). We then compared squirrel monkeys' performance to existing data on capuchin monkeys (Sapajus [Cebus] apella), a closely related species that routinely cooperates, to determine what, if any, differences in decision making emerged. Some pairs of both species found the payoff-dominant Nash Equilibrium (NE) in the coordination game, but failed to find the NE in subsequent games. Our results suggest that, like capuchins, squirrel monkeys coordinate their behavior with others, suggesting that such mutual outcomes occur in at least some contexts, even in species that do not routinely cooperate.
Games derived from experimental economics can be used to directly compare decision-making behavior across primate species, including humans. For example, the use of coordination games, such as the Assurance game, has shown that a variety of primate species can coordinate; however, the mechanism by which they do so appears to differ across species. Recently, these games have been extended to explore anti-coordination and cooperation in monkeys, with evidence that they play the Nash equilibria in sequential games in these other contexts. In the current paper, we use the same methods to explore chimpanzees' behavior in the Assurance Game; an anti-coordination game, the Hawk Dove game; and a cooperation game with a temptation to defect, the Prisoner's Dilemma game. We predicted that they would consistently play the Nash equilibria, as do the monkeys, and that, as in previous work, the subjects' level of experience with cognitive experiments would impact performance. Surprisingly, few of our pairs consistently played the same outcome (i.e., no statistically significant preferences), although those who did showed evidence consistent with Nash equilibria play, the same pattern seen more consistently in the monkeys. We consider reasons for their inconsistent performance; for instance, perhaps it was due to lack of interest in a task that rewarded them almost every trial no matter what option they chose, although this does not explain why they were inconsistent when the monkeys were not. A second goal of our study was to ascertain the effects of exogenous oxytocin in their decision making in one population. In line with recent work showing complex effects of oxytocin on social behavior, we found no effect on subjects' outcomes. We consider possible explanations for this as well.
Language, humans’ most distinctive trait, still remains a ‘mystery’ for evolutionary theory. It is underpinned by a universal infrastructure — cooperative turn-taking — which has been suggested as an ancient mechanism bridging the existing gap between the articulate human species and their inarticulate primate cousins. However, we know remarkably little about turn-taking systems of nonhuman animals, and methodological confounds have often prevented meaningful cross-species comparisons. Thus, the extent to which cooperative turn-taking is uniquely human or represents a homologous and/or analogous trait is currently unknown. The present paper draws attention to this promising research avenue by providing an overview of the state of the art of turn-taking in four animal taxa — birds, mammals, insects and anurans. It concludes with a new comparative framework to spur more research into this research domain and test which elements of the human turn-taking system are shared across species and taxa.
Cooperatively breeding common marmosets show substantial variation in the amount of help they provide. Pay-to-stay and social prestige models of helping attribute this variation to audience effects, i.e. that individuals help more if group members can witness their interactions with immatures, whereas models of kin selection, group augmentation or those stressing the need to gain parenting experience do not predict any audience effects. We quantified the readiness of adult marmosets to share food in the presence or absence of other group members. Contrary to both predictions, we found a reverse audi- ence effect on food-sharing behaviour: marmosets would systematically share more food with immatures when no audience was present. Thus, helping in common marmosets, at least in related family groups, does not support the pay-to-stay or the social prestige model, and helpers do not take advantage of the opportunity to engage in reputation management. Rather, the results appear to reflect a genuine concern for the immatures’ well-being, which seems particularly strong when solely responsible for the immatures.
Chimpanzees and bonobos are highly capable of tracking other’s mental states. It has been proposed, however, that in contrast to humans, chimpanzees are only able to do this in competitive interactions but this has rarely been directly tested. Here, pairs of chimpanzees or bonobos (Study 1) and 4-year-old children (Study 2) were presented with two almost identical tasks differing only regarding the social context. In the cooperation condition, players’ interests were matched: they had to make corresponding choices to be mutually rewarded. To facilitate coordination, subjects should thus make their actions visible to their partner whose view was partially occluded. In the competition condition, players’ interests were directly opposed: the partner tried to match the subject’s choice but subjects were only rewarded if they chose differently, so that they benefited from hiding their actions. The apes successfully adapted their decisions to the social context and their performance was markedly better in the cooperation condition. Children also distinguished between the two contexts, but somewhat surprisingly, performed better in the competitive condition. These findings demonstrate experimentally that chimpanzees and bonobos can take into account what others can see in cooperative interactions. Their social-cognitive skills are thus more flexible than previously assumed.
Social animals need to coordinate with others to reap the benefits of groupliving even when individuals’ interests are misaligned. We compare how chimpanzees, bonobos and children coordinate their actions with a conspecific in a Snowdrift game, which provides a model for understanding how organisms coordinate and make decisions under conflict. In study 1, we presented pairs of chimpanzees, bonobos and children with an unequal reward distribution. In the critical condition, the preferred reward could only be obtained by waiting for the partner to act, with the risk that if no one acted, both would lose the rewards. Apes and children successfully coordinated to obtain the rewards. Children used a ‘both-partner-pull’ strategy and communicated during the task, while some apes relied on an ‘only-one-partner-pulls’ strategy to solve the task, although therewere also signs of strategic behaviour as they waited for their partner to pull when that strategy led to the preferred reward. In study 2, we presented pairs of chimpanzees and bonobos with the same set-up as in study 1 with the addition of a non-social option that provided them with a secure reward. In this situation, apes had to actively decide between the unequal distribution and the alternative. In this set-up, apes maximized their rewards by taking their partners’ potential actions into account. In conclusion, children and apes showed clear instances of strategic decision-making to maximize their own rewards while maintaining successful coordination. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
Humans constantly have to coordinate their decisions with others even when their interests are conflicting (e.g., when 2 drivers have to decide who yields at an intersection). So far, however, little is known about the development of these abilities. Here, we present dyads of 5-year-olds (N = 40) with a repeated chicken game using a novel methodology: Two children each steered an automated toy train carrying a reward. The trains simultaneously moved toward each other so that in order to avoid a crash—which left both children empty-handed—1 train had to swerve. By swerving, however, the trains lost a portion of the rewards so that it was in each child’s interest to go straight. Children coordinated their decisions successfully over multiple rounds, and they mostly did so by taking turns at swerving. In dyads in which turn-taking was rare, dominant children obtained significantly higher payoffs than their partners. Moreover, the coordination process was more efficient in turn-taking dyads as indicated by a significant reduction in conflicts and verbal protest. These findings indicate that already by the late preschool years children can independently coordinate decisions with peers in recurrent conflicts of interest.
Even when hunting in groups is mutually beneficial, it is unclear how communal hunts are initiated. If it is costly to be the only hunter, individuals should be reluctant to hunt unless others already are.We used 70 years of data from three communities to examine how male chimpanzees ‘solve’ this apparent collective action problem. The ‘impact hunter’ hypothesis proposes that group hunts are sometimes catalysed by certain individuals that hunt more readily than others. In two communities (Kasekela and Kanyawara),we identified a total of five males that exhibited high hunt participation rates for their age, and whose presence at an encounter with red colobus monkeys increased group hunting probability. Critically, these impact hunters were observed to hunt first more often than expected by chance.We argue that by hunting first, these males dilute prey defences and create opportunities for previously reluc- tant participants. This by-product mutualism can explain variation in group hunting rates within and between social groups. Hunting rates declined after the death of impact hunter FG in Kasekela and after impact hunter MS stopped hunting frequently in Kanyawara. There were no impact hunters in the third, smaller community (Mitumba), where, unlike the others, hunting probability increased
Parenting patterns range widely among human and nonhuman primates. Rarely do single mothers parent without help. Many female-bonded species have female relatives (grandmothers and aunts) to help with infant care. In other species both parents assist in infant care, or there is cooperative care where several group members work together to rear a single infant or litter. Cooperative care is relatively uncommon in primates, but is found in many birds and in some non-primate mammals such as wolves and meerkats. In primates, cooperative care is seen primarily in marmosets and tamarins, small monkeys from the New World. We first describe patterns of cooperative care of infants in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus). Then we exam- ine the cooperative care family as a social system describing the mechanisms that main- tain relationships among family members to maintain cooperative care. Human beings also require cooperative care due to the long duration of infancy and childhood, so we conclude with some speculations about how cooperative care benefits children and how research with cooperative care primates might help us to become more successful parents. Growing Up Cooperatively Childcare in mammals is often studied and discussed only in the context of mother-infant interactions because mothers bear the costs of gestation and lactation. Occasionally there are studies on fathers and the role they play in infant care. Rarely is infant care and infant development studied in the context of families and the contri- butions that each family member might make to successful infant care. The animal models that are used to study parenting are typically species where mothers alone are responsible for all infant care (e.g., rats, Fleming, 1996; vervet monkeys, Fairbanks,
The importance of between-group competition in the social evolution of animal societies is controversial, particularly with respect to understanding the origins and maintenance of cooperation in our own species. Among primates, aggressive between-group encounters are often rare or strikingly absent, a phenomenon that in some species has been ascribed to the presence of collective action problems. Here, we report on a series of comparative tests that show that the intensity of between-group contest competition is indeed lower in species that experience a collective action problem while controlling for predictions from an “ideal gas” model of animal encounters and general species’ ecology. Species that do not succumb to the collective action problem are either cooperative breeders, are characterized by philopatry of the dominant sex, or live in relatively small groups with few individuals of this dominant sex. This implies that collective action problems are averted either through shared genes and benefits or a by-product mutualism in which the territorial behavior of some privileged individuals is not affected by the behavior of others. We conclude that across the primate taxon, the intensity of between-group competition is predominantly constrained by a social dilemma among group members, rather than ecological conditions, and that the collective action problem is thus an important selective pressure in the evolution of primate (including human) cooperation and sociality.
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.
Tamarins (Callitrichidae) are cooperative breeders. Groups typically contain only two or three breeding individuals and subordinate group members are reproductively suppressed. Nonreproductive individuals, which are usually the offspring of the group's breeding members, delay dispersal while providing care to infant siblings. Callitrichid breeder-infant and helper-infant relationships have been well studied but empirical studies regarding the dynamics of breeder-helper relationships are sparse. I examined food-transfer interactions among parents and natal adults in 7 groups of captive lion tamarins, Leontopithecus spp., to test whether relationships are maintained by mutualism or reciprocity or are to the benefit of one side of a dyad. Individuals that had recently received food from a group member most frequently released food to the previous donor as their next act of transfer. Conversely, food transfer was not dependent on symmetrical relationships within groups over a time frame of several weeks. These results suggest that mutualism plays a role in the maintenance of food-transfer relationships but reciprocity does not. However, there is evidence for a reciprocal relationship between grooming and food transfer in one group. Subadults and adults living in their natal groups transferred proportionally more food to mothers than to oppositely-sexed subadult and adult siblings. Thus, individuals most likely to receive aggression preferentially released food to individuals most likely to inflict injury upon them. Although these results support the coercion hypothesis, they may suggest alternatively that food transfer by helpers to breeding adults is driven by inclusive fitness considerations.
Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent-offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event-food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother-infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.
The intense arousal and excitement shown by adult male chimpanzees, Pan troglodytes, during territorial attacks on other chimpanzees and predation upon monkeys suggest that similar psychological mechanisms may be involved. Specifically, it has been proposed that hunting behaviour in chimpanzees evolved from intraspecies aggression. Over 32 years, chimpanzees at Gombe National Park, Tanzania were significantly more likely to engage in a territorial border patrol on days when they hunted red colobus monkeys (Procolobus spp.), and vice versa, even after statistically controlling for male chimpanzee party size.We test the hypothesis that this correlation arises because hunting and patrolling are components of a species-level aggressive behavioural syndrome; specifically that predation arose as a by-product of territorial aggression in this species. However, hunting was equally likely to occur after a patrol and/or an intergroup interaction as it was before, and the occurrence of an intergroup interaction in which the chimpanzees approached strangers did not increase subsequent hunting probability.We also reject the hypothesis that hunting and patrolling reflect an individual-level behavioural syndrome. We identified two ‘impact hunters’ whose presence increased hunting probability. Similarly, there were also three ‘impact patrollers’, who increased the likelihood that a visit to the periphery of the community range resulted in a patrol. While this discovery has important implications for our understanding of the proximate causes of cooperation, it does not explain the temporal correlation between patrolling and hunting, since no males had such an impact in both contexts. Instead, the data suggest that the correlation arose because patrols typically involved males travelling long distances, which increased the probability of encountering prey. Additionally, parties that travelled to the periphery were more likely to encounter colobus in woodland, where hunts are more likely to occur and to succeed. Therefore, we conclude that ecological, rather than psychological, factors promote the co-occurrence of hunting and territorial aggression in this species.
Infant marmosets and tamarins (Callitrichidae) frequently receive food from older group members. Three possible functions of food sharing in lion tamarins were examined experimentally. The first hypothesis, that food sharing ensures that infants receive sufficient food even if it is difficult for them to acquire it themselves, was tested by varying the ease with which infants could reach a food source. When access to food was restricted, infants fed themselves less, received more food from others, and had a higher success rate in begging attempts. The second hypothesis, that food sharing helps teach infants an appropriate diet, was tested by presenting fruits that were novel to infants. Although infants fed themselves less under these conditions, adults were less likely to share novel foods than familiar foods. The final experiment compared food sharing when food was abundant with behavior when food items were presented singly. Infants fed themselves less and received more food from others when food items were rare. These results suggest that food sharing in lion tamarins helps to ensure that infants receive adequate amounts of food which is difficult to locate or acquire, but that it is not involved in teaching infants which foods they should eat. © 1993 Wiley-Liss, Inc.
Human infants rely on social interactions to acquire food-related information.1, 2 Adults actively teach children about food through culturally diverse feeding practices. Characteristics we share with the other primates, such as complex diets, highly social lives, and extended juvenile periods, suggest that social learning may be important during ontogeny throughout the order. Although all young primates typically pay attention to feeding adults, great apes and callitrichids, in particular, acquire new foraging techniques through abilities unknown in other nonhuman primates; that is, they learn by imitation. However, ape social learning is almost exclusively infant-initiated, while adult callitrichids actively teach their young. It is unlikely that the same selective forces have acted to favor sophisticated social-learning mechanisms in both taxa.3, 4 Equipped with an ape brain, complex foraging methods, and a cooperative infant-care system, early hominins were uniquely poised to take social learning about food and foraging techniques to a new level.
Reciprocity is a ubiquitous and important human trait. Still, the evolutionary origin is largely unclear, partly because it is believed that our closest living relatives, other primates, do not reciprocate help. Consequently, reciprocity is suggested to have evolved in the human linage only. However, our systematic review of studies investigating reciprocity in non-human primates revealed that, contrary to common perception, there are more positive than negative findings in both experimental and observational studies. Furthermore, we argue that negative findings can provide important insights. We found that reciprocity is not confined to unrelated individuals. In addition, reciprocity can be influenced by the choice of experimental design, relationship quality, social services and temporal scales. Thus, negative findings should not be used as evidence of no reciprocity but as the building blocks for a more comprehensive theory. Based on our review, we conclude that reciprocity in primates is present but underestimated. We close by suggesting further steps that could pave the way for future research aimed at understanding the evolutionary origins of reciprocity.
Comparative approaches to experimental economics have shed light on the evolution of social decision‐making across a range of primate species, including humans. Here we replicate our previous work looking at six pairs of capuchin monkeys' (Sapajus [Cebus] apella) responses to scenarios requiring both coordination (Assurance Game) and anti‐coordination (Hawk‐Dove Game). This then provides a foundation for assessing their responses to two additional games, one with a scenario of beneficial cooperation with a temptation to defect (Prisoner's Dilemma) and one with an environment requiring changing strategies within short temporal proximity (Alternating Economic Game). We additionally explored the effects of exogenous oxytocin on decision‐making. Oxytocin did not affect decisions in any of our games. Results from the first two games largely replicated our previous findings. Responses to the Prisoner's Dilemma were more varied than was seen in previous games, with pairs respectively cooperating, defecting, and failing to establish stable strategies. Such variability indicates that this game may be a good assay for individual differences in social decision‐making. Finally, capuchins were able to flexibly switch between their previously established strategies within each of the different games, even when the games were presented within the same session, requiring strategy adjustments within short temporal proximity. These results build on earlier findings showing that capuchins can alter decision‐making strategies as the context demands, which is likely essential for decision‐making in naturally occurring contexts.
Research Highlights
• Capuchins found strategies in the Assurance and Hawk‐Dove Games but not in a Prisoner's Dilemma
• Subjects successfully alternated strategies between games presented in the same session
• Oxytocin did not influence decision‐making in any of the games
One of the goals of studying primate social cognition is to better understand how decision-making is similar or different across primate species, including humans. Recently, researchers have begun to use paradigms from experimental economics that allow for direct comparisons across species using identical or highly similar experimental approaches. In many cases, paradigms used extensively in humans, such as the Assurance Game, Matching Pennies Game, and Prisoner’s Dilemma, have been adapted for other species in order to understand how different payoff structures influence decision-making. This approach has been utilized to explore not only individual differences and the influence of the social environment on behavior, but also the ecological relevance of such paradigms to the species in question. This comprehensive exploration allows for the most robust understanding of the evolution and development of social decision-making.
Cooperation often comes with the temptation to defect and benefit at the cost of others. This tension between cooperation and defection is best captured in social dilemmas like the Prisoner’s Dilemma. Adult humans have specific strategies to maintain cooperation during Prisoner’s Dilemma interactions. Yet, little is known about the ontogenetic and phylogenetic origins of human decision-making strategies in conflict scenarios. To shed light on this question, we compared the strategies used by chimpanzees and 5-year old children to overcome a social dilemma. In our task, waiting for the partner to act first produced the best results for the subject. Alternatively, they could mutually cooperate and divide the rewards. Our findings indicate that the two species differed substantially in their strategies to solve the task. Chimpanzees became more strategic across the study period by waiting longer to act in the social dilemma. Children developed a more efficient strategy of taking turns to reciprocate their rewards. Moreover, children used specific types of communication to coordinate with their partners. These results suggest that while both species behaved strategically to overcome a conflict situation, only children engaged in active cooperation to solve a social dilemma.
Proximate factors of primate food sharing, in contrast to its evolutionary explanations, have received little attention. Active food sharing is considered prosocial, since possessors may benefit others by spontaneously passing food or by reacting to ‘signals of need’. However, in contrast to passive sharing, active food sharing is rare in most nonhuman primates. Surprisingly, previous research showed that captive Sumatran orang-utans actively share food more frequently than chimpanzees and bonobos, and hence, appear more prosocial. Yet these comparisons with the two Pan species were relying on previously published studies, which differed with regard to methods and food types used. Here we used the identical procedure and food type to compare the food-sharing behaviour of 10 captive Sumatran orang-utans and 18 chimpanzees, in situations where individuals could monopolize a sharable food source. We focused on communicative behaviours used to initiate food transfers, and assessed whether and how much food was transferred in response to these initiation attempts. In both species, most transfers were initiated by taking the food, resulting in passive sharing, while active sharing by offering food or after requesting it occurred only rarely. However, orang-utans differed from chimpanzees in several aspects. Because the food was mostly monopolized by the adult male, orang-utans attempted to initiate food transfers more frequently, resisted more to taking attempts, and were less likely to transfer whole food items. In both species, requests were less likely to result in food transfers, indicating that in situations involving access to food, they do not necessarily respond to ‘signals of need’. We argue that in addition to instances of active sharing, other factors such as the degree of food monopolization, response rates to ‘signals of need’, and the quality and quantity of transferred food need to be considered to gain a more detailed picture of prosociality across species.
To better understand the evolutionary history of human decision-making, we compare human behavior to that of two monkey species in a symmetric game of conflict with two asymmetric equilibria. While all of these species routinely make decisions in the context of social cooperation and competition, they have different socio-ecologies, which leads to different predictions about how they will respond. Our prediction was that anti-matching would be more difficult than matching in a symmetric coordination with simultaneous moves. To our surprise, not only do rhesus macaques frequently play one asymmetric Nash equilibrium, but so do capuchin monkeys, whose play in the coordination game was literally not distinguishable from randomness (in simultaneous play). Humans are the only species to play both asymmetric equilibria in a repeated game.
Nature may be red in tooth and claw, but working together with one’s group mates can be an efficient way to increase fitness. Cooperation is common, for example, among capuchin monkeys. These monkeys are not only willing to help others obtain resources, but are more likely to share with individuals who help them. Cooperation can be risky, however, and not surprisingly capuchins are much less likely to cooperate when a partner is able to monopolize the reward. However, they also pay attention to the partner’s behavior; monkeys that share with their partners promote successful cooperation, and thus actually receive more benefits over the long term than those who always claim the best rewards for themselves. The ability to recognize inequity may be a mechanism by which the monkeys determine which partners are the best collaborators. The study of capuchin monkeys can tell us quite a lot about how, when, and with whom to cooperate, perhaps providing insight into the design and implementation of our own human cooperative institutions.
Long-term collaborative relationships require that any jointly produced resources be shared in mutually satisfactory ways. Prototypically, this sharing involves partners dividing up simultaneously available resources, but sometimes the collaboration makes a resource available to only one individual, and any sharing of resources must take place across repeated instances over time. Here, we show that beginning at 5 years of age, human children stabilize cooperation in such cases by taking turns across instances of obtaining a resource. In contrast, chimpanzees do not take turns in this way, and so their collaboration tends to disintegrate over time. Alternating turns in obtaining a collaboratively produced resource does not necessarily require a prosocial concern for the other, but rather requires only a strategic judgment that partners need incentives to continue collaborating. These results suggest that human beings are adapted for thinking strategically in ways that sustain long-term cooperative relationships and that are absent in their nearest primate relatives.
Some problems of resource distribution can be solved on equal terms only by taking turns. We presented such a problem to 168 pairs of 5- to 10-year-old children from one Western and two non-Western societies (German, Samburu, Kikuyu). Almost all German pairs solved the problem by taking turns immediately, resulting in an equal distribution of resources throughout the game. In the other groups, one child usually monopolized the resource in Trial 1 and sometimes let the partner monopolize it in Trial 2, resulting in an equal distribution in only half the dyads. These results suggest that turn-taking is not a natural strategy uniformly across human cultures, but rather that different cultures use it to different degrees and in different contexts.
The snowdrift game is a model for studying social coordination in the context of competing interests. We presented pairs of chimpanzees with a situation in which they could either pull a weighted tray together or pull alone to obtain food. Ultimately chimpanzees should coordinate their actions because if no one pulled, they would both lose the reward. There were two experimental manipulations: the tray's weight (low or high weight condition) and the time to solve the dilemma before the rewards became inaccessible (40 seconds or 10 seconds). When the costs were high (i.e high weight condition), chimpanzees waited longer to act. Cooperation tended to increase in frequency across sessions. The pulling effort invested in the task also became more skewed between subjects. The subjects also adjusted their behaviour by changing their pulling effort for different partners. These results demonstrate that chimpanzees can coordinate their actions in situations where there is a conflict of interest.
The neurohormone oxytocin (OT) is positively involved in the regulation of parenting and social bonding in mammals, and may thus also be important for the mediation of alloparental care. In cooperatively breeding marmosets, infants are raised in teamwork by parents and adult and sub-adult non-reproductive helpers (usually older siblings). Despite high intrinsic motivation, which may be mediated by hormonal priming, not all individuals are always equally able to contribute to infant-care due to competition among care-takers. Among the various care-taking behaviors, proactive food sharing may reflect motivational levels best, since it can be performed ad libitum by several individuals even if competition among surplus care-takers constrains access to infants. Our aim was to study the link between urinary OT levels and care-taking behaviors in group-living marmosets, while taking affiliation with other adults and infant age into account. Over eight reproductive cycles, 26 individuals were monitored for urinary baseline OT, care-taking behaviors (baby-licking, -grooming, -carrying, and proactive food sharing), and adult-directed affiliation. Mean OT levels were generally highest in female breeders and OT increased significantly in all individuals after birth. During early infancy, high urinary OT levels were associated with increased infant-licking but low levels of adult-affiliation, and during late infancy, with increased proactive food sharing. Our results show that, in marmoset parents and alloparents, OT is positively involved in the regulation of care-taking, thereby reflecting the changing needs during infant development. This particularly included behaviors that are more likely to reflect intrinsic care motivation, suggesting a positive link between OT and motivational regulation of infant-care.
Reciprocity is probably the most debated of the evolutionary explanations for cooperation. Part of the confusion surrounding this debate stems from a failure to note that two different processes can result in reciprocity: partner control and partner choice. We suggest that the common observation that group-living animals direct their cooperative behaviours preferentially to those individuals from which they receive most cooperation is to be interpreted as the result of the sum of the two separate processes of partner control and partner choice. We review evidence that partner choice is the prevalent process in primates and propose explanations for this pattern. We make predictions that highlight the need for studies that separate the effects of partner control and partner choice in a broader variety of group-living taxa.
A solution is suggested for an old unresolved social psychological problem.
When testing primates with cognitive tasks, it is usually not considered that subjects differ markedly in terms of emotional reactivity toward the experimenter, which potentially affects a subject's cognitive performance. We addressed this issue in common marmosets (Callithrix jacchus), a monkey species in which males tend to show stronger emotional reactivity in testing situations, whereas females have been reported to outperform males in cognitive tasks. In a two-phase experiment, we first quantified the emotional reactivity of 14 subjects toward four different experimenters performing a standardized behavioral action sequence and then assessed whether and how it affected the subjects' participation and performance in a subsequent object permanence task. A test session was terminated if a subject refused to make a choice in four consecutive trials. Highly emotionally aroused individuals, particularly males, were less likely to participate in the cognitive task and completed fewer trials. However, whenever they did participate and were attentive to the task, their performance was not affected. Our results suggest that differences in emotional reactivity toward an experimenter have no major impact on cognitive performance if strict criteria are applied on when to abandon a test session and if performance is corrected for attention to the test procedure. Furthermore, they suggest that the reported sex differences in cognitive performance in marmosets may be owing to motivational and attentional factors, rather than a difference in cognitive ability per se.
The involvement of parents and siblings in infant care in similarly composed groups of common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus) was compared during the infants' first 8 weeks of life. The results indicate an earlier infant independence in C. jacchus than in S. oedipus due primarily to a more frequent rejection of carried infants in C. jacchus. There was no species difference in extent of maternal involvment in carrying infants. However, S. oedipus fathers carried infants significantly more often during weeks 5–8 than did C. jacchus fathers. Siblings were generally more involved in infant care at an earlier infant age in C. jacchus than in S. oedipus.
A model for the evolution of cooperation shows that two conditions are necessary for cooperation to be stable: a hunting success rate that is low for single hunters and increases with group size, and a social mechanism limiting access to meat by non-hunters. Testing this model on Taı̈ chimpanzees, Pan troglodytes, showed that (1) it pays for individuals to hunt in groups of three or four rather than alone or in pairs, and (2) cooperation is stable because hunters gain more at these group sizes than cheaters, owing to a meat-sharing pattern in which hunting, dominance and age, in that order, determine how much an individual gets. In addition, hunters provide cheaters (about 45% of the meat eaters) with the surplus they produce during the hunts. Thus, cooperation in Taı̈ male chimpanzees is an evolutionarily stable strategy, and its success allows cheating to be an evolutionarily stable strategy for Taı̈ female chimpanzees. In Gombe chimpanzees, cooperation is not stable, first, because hunting success is very high for single hunters, and second, because no social mechanism exists that limits access to meat by non-hunters. The analysis showed that some assumptions made when discussing cooperation in other social hunters might be wrong. This might downgrade our general perception of the importance of cooperation as an evolutionary cause of sociality.
Fourteen adult male/female pairs of tamarins, 5 red-chested (Saguinus labiatus) 5 saddle-back (S. fuscicollis) and 4 cotton-top (S. oedipus) were each given a series of foraging tasks in which the monkeys reached in to unfamiliar boxes to take food. Behaviour was recorded that related directly to the tasks. In addition, observations were made before each task presentation and compared with equivalent behaviour during the tasks. S. fuscicollis differed significantly from the other species in the baseline conditions and in the presence of the tasks, which they approached less frequently and for less time. Further, males and females across all species differed significantly in that females attempted the tasks more frequently, they spent longer periods attempting to solve them, and they removed food more often. These results were considered as evidence for male ‘deference’ to a potentially reproductive female.
Neotropical primates show a remarkable range in body size, spanning two orders of magnitude from the tiny pygmy marmosets (100 g) to the woolly spider monkeys (11,000+ g). Even among the “smaller” platyrrhines, the range is large. In addition, these primates demonstrate a wide diversity in degrees and directions of sexual dimorphism, in both body size and canine size, from marked positive dimorphism (males larger than females), through monomorphic species, to negative dimorphism. Potential correlates or causes of the patterns of dimorphism in body size are investigated, including overall body size, natural selection for life history strategies, sexual selection, diet, habitat, and phylogenetic inertia. Focus is especially on those genera that show species-specific variation in dimorphism (e.g., Saguinus, Pithecia). Results are contrary to those for cross-primate or catarrhine studies, but complementary to recent studies on strepsirhines. They suggest that sexual selection is the primary determinant of degree and pattern of sexual dimorphism in platyrrhines, but that there is also a dietary effect. Natural selection may have some effect, although not the parameters analyzed here. Body size, habitat (primary vs. secondary forest preference), and phylogenetic inertia or constraints do not have any effect on the presence of sexual dimorphism in body weights in New World monkeys. © 1994 Wiley-Liss, Inc.
This chapter discusses the current knowledge of competition and cooperation in wild chimpanzees. It explicitly focuses on recent field studies that shed new light on how chimpanzees compete, cooperate, and cooperate to compete. It outlines the social, demographic, and ecological contexts within which wild chimpanzees compete and cooperate. Within groups, males compete over status and access to fecundable females. High-ranking males gain clear reproductive benefits as they monopolize mating with females when they are most likely to conceive. Rank striving also incurs significant physiological costs, and the extent to which these are mitigated by survival benefits, such as increased access to resources, is not clear. Males direct frequent aggression against females, much of which appears to function as sexual coercion, decreasing the chance that a female will mate with other males. Females are aggressive primarily in the context of feeding competition. Despite evidence that female rank has important effects on reproduction, aggression by parous females against other parous females is rare, and female dominance ranks are stable over long periods of time. Intergroup relations among chimpanzees are predictably hostile. The evolutionary mechanisms that account for chimpanzee cooperation require further study. Current data suggest little role for kin selection. Some patterns of exchange are suggestive of reciprocal altruism, but better data are required to rule out the alternative hypothesis of mutualism.
In Parque Nacional Manuel Antonio, Costa Rica, an adult male Cebus capucinus was observed repeatedly hitting a venomous snake (Bothropsasper) with a branch. Initially a large dead branch overhanging the snake had been broken off in the course of aggressive displays to the snake by the adult and two subadult males. The snake's escape was apparently prevented by the weight of the fallen branch and possibly by the injuries caused by its fall. This is the first direct observation of a capuchin monkey in a natural habitat using a tool.
Prosocial decisions may lead to unequal payoffs among group members. Although an aversion to inequity has been found in empirical studies of both human and nonhuman primates, the contexts previously studied typically do not involve a trade-off between prosociality and inequity. Here we investigate the apparent coexistence of these two factors, specifically the competing demands of prosociality and equity. We directly compare the responses of brown capuchin monkeys (Cebus apella) among situations where prosocial preferences conflict with equality, using a paradigm comparable to other studies of cooperation and inequity in this species. By choosing to pull a tray towards themselves, subjects rewarded themselves and/or another in conditions in which the partner either received the same or different rewards, or the subject received no reward. In unequal payoff conditions, subjects could obtain equality by choosing not to pull in the tray, so that neither individual was rewarded. The monkeys showed prosocial preferences even in situations of moderate disadvantageous inequity, preferring to pull in the tray more often when a partner was present than absent. However, when the discrepancy between rewards increased, prosocial behavior ceased.
Cooperation is common across nonhuman animal taxa, from the hunt-ing of large game in lions to the harvesting of building materials in ants. Theorists have proposed a number of models to explain the evolution of cooperative behavior. These ultimate explanations, however, rarely consider the proximate constraints on the im-plementation of cooperative behavior. Here we review several types of cooperation and propose a suite of cognitive abilities required for each type to evolve. We propose that several types of cooperation, though theoretically possible and functionally adaptive, have not evolved in some animal species because of cognitive constraints. We argue, therefore, that future modeling efforts and experimental investigations into the adaptive function of cooperation in animals must be grounded in a realistic assessment of the psychological ingredients required for cooperation. Such an approach can account for the puzzling distribution of cooperative behaviors across taxa, especially the seemingly unique occurrence of cooperation observed in our own species.
Humans can engage in relatively indiscriminate altruistic behaviors such as donating money to charities, giving blood, and volunteering to review scientific papers. They also live in societies characterized by examples of cooperation of unmatched complexity, such as organized armies, the cooperative building of infrastructures such as roads and railways, and tax-paying, among others. (We exclude, of course, the “anonymous” societies of some social insects in which the animals themselves are not aware of the cooperative roles they play.) The emphasis on these unique aspects of our behavior1 has sometimes distracted scientists from paying attention to the more common aspects of our daily lives, which share characteristics with those of our fellow primates. We invite friends for dinner, console others after a loss, intervene in ongoing fights, and even groom others.2–4 These small acts of altruism, which constitute a large part of our daily social life, tend to resemble those of nonhuman primates.