The evolution of altruistic social preferences in human groups

In this paper, we consider three hypotheses to account for the evolution of the extraordinary capacity for large-scale cooperation and altruistic social preferences within human societies. One hypothesis is that human cooperation is built on the same evolutionary foundations as cooperation in other animal societies, and that fundamental elements of the social preferences that shape our species'' cooperative behaviour are also shared with other closely related primates. Another hypothesis is that selective pressures favouring cooperative breeding have shaped the capacity for cooperation and the development of social preferences, and produced a common set of behavioural dispositions and social preferences in cooperatively breeding primates and humans. The third hypothesis is that humans have evolved derived capacities for collaboration, group-level cooperation and altruistic social preferences that are linked to our capacity for culture. We draw on naturalistic data to assess differences in the form, scope and scale of cooperation between humans and other primates, experimental data to evaluate the nature of social preferences across primate species, and comparative analyses to evaluate the evolutionary origins of cooperative breeding and related forms of behaviour.     

Culture and the evolution of human cooperation

The scale of human cooperation is an evolutionary puzzle. All of the available evidence suggests that the societies of our Pliocene ancestors were like those of other social primates, and this means that human psychology has changed in ways that support larger, more cooperative societies that characterize modern humans. In this paper, we argue that cultural adaptation is a key factor in these changes. Over the last million years or so, people evolved the ability to learn from each other, creating the possibility of cumulative, cultural evolution. Rapid cultural adaptation also leads to persistent differences between local social groups, and then competition between groups leads to the spread of behaviours that enhance their competitive ability. Then, in such culturally evolved cooperative social environments, natural selection within groups favoured genes that gave rise to new, more pro-social motives. Moral systems enforced by systems of sanctions and rewards increased the reproductive success of individuals who functioned well in such environments, and this in turn led to the evolution of other regarding motives like empathy and social emotions like shame.     

From social network (centralized vs. decentralized) to collective decision-making (unshared vs. shared consensus)

Relationships we have with our friends, family, or colleagues influence our personal decisions, as well as decisions we make together with others. As in human beings, despotism and egalitarian societies seem to also exist in animals. While studies have shown that social networks constrain many phenomena from amoebae to primates, we still do not know how consensus emerges from the properties of social networks in many biological systems. We created artificial social networks that represent the continuum from centralized to decentralized organization and used an agent-based model to make predictions about the patterns of consensus and collective movements we observed according to the social network. These theoretical results showed that different social networks and especially contrasted ones--star network vs. equal network--led to totally different patterns. Our model showed that, by moving from a centralized network to a decentralized one, the central individual seemed to lose its leadership in the collective movement's decisions. We, therefore, showed a link between the type of social network and the resulting consensus. By comparing our theoretical data with data on five groups of primates, we confirmed that this relationship between social network and consensus also appears to exist in animal societies.     

Cooperation and human cognition: the Vygotskian intelligence hypothesis

Nicholas Humphrey's social intelligence hypothesis proposed that the major engine of primate cognitive evolution was social competition. Lev Vygotsky also emphasized the social dimension of intelligence, but he focused on human primates and cultural things such as collaboration, communication and teaching. A reasonable proposal is that primate cognition in general was driven mainly by social competition, but beyond that the unique aspects of human cognition were driven by, or even constituted by, social cooperation. In the present paper, we provide evidence for this Vygotskian intelligence hypothesis by comparing the social-cognitive skills of great apes with those of young human children in several domains of activity involving cooperation and communication with others. We argue, finally, that regular participation in cooperative, cultural interactions during ontogeny leads children to construct uniquely powerful forms of perspectival cognitive representation.     

Testing the Cognition of the Forgotten Colobines: A First Look at Golden Snub-Nosed Monkeys (Rhinopithecus roxellana)

Although our understanding of primate cognition is growing rapidly, little is known about the cognition of colobines. Here we report the results of a set of 5 experiments on colobine cognition using 17 golden snub-nosed monkeys (Rhinopithecus roxellana). These monkeys are folivores that form multilevel societies with groups of hundreds of individuals and relatively high fission–fusion dynamics. We investigated their sensitivity to human social cues and ability to inhibit impulsive behavioral responses. In three sociocognitive experiments we found that, like most other primates, they follow the gaze direction of a human demonstrator but there is no evidence that they use others’ social cues in a cooperative task to locate hidden food or in a competitive task to steal forbidden food. In two inhibitory control experiments, we found that the monkeys showed a low level of inhibitory control, comparable to that of other folivorous primates. These results suggest that phylogeny and folivory might have been important in shaping the cognition of golden snub-nosed monkeys. Moreover, this species’ large group size and relatively high fission–fusion dynamics may not have imposed a significant social challenge to their cognition, as social interactions occur mainly within basic social units.     

The psychology of primate cooperation and competition: a call for realigning research agendas

Cooperation and competition are two key components of social life. Current research agendas investigating the psychological underpinnings of competition and cooperation in non-human primates are misaligned. The majority of work on competition has been done in the context of theory of mind and deception, while work on cooperation has mostly focused on collaboration and helping. The current impression that theory of mind is not necessarily implicated in cooperative activities and that helping could not be an integral part of competition might therefore be rather misleading. Furthermore, theory of mind research has mainly focused on cognitive aspects like the type of stimuli controlling responses, the nature of representation and how those representations are acquired, while collaboration and helping have focused primarily on motivational aspects like prosociality, common goals and a sense of justice and other-regarding concerns. We present the current state of these two bodies of research paying special attention to how they have developed and diverged over the years. We propose potential directions to realign the research agendas to investigate the psychological underpinnings of cooperation and competition in primates and other animals.     

The evolution of daily food sharing: A Bayesian phylogenetic analysis

Some human subsistence economies are characterized by extensive daily food sharing networks, which may buffer the risk of shortfalls and facilitate cooperative production and divisions of labor among households. Comparative studies of human food sharing can assess the generalizability of this theory across time, space, and diverse lifeways. Here we test several predictions about daily sharing norms–which presumably reflect realized cooperative behavior–in a globally representative sample of nonindustrial societies (the Standard Cross-Cultural Sample), while controlling for multiple sources of autocorrelation among societies using Bayesian multilevel models. Consistent with a risk-buffering function, we find that sharing is less likely in societies with alternative means of smoothing production and consumption such as animal husbandry, food storage, and external trade. Further, food sharing was tightly linked to labor sharing, indicating gains to cooperative production and perhaps divisions of labor. We found a small phylogenetic signal for food sharing (captured by a supertree of human populations based on genetic and linguistic data) that was mediated by food storage and social stratification. Food sharing norms reliably emerge as part of cooperative economies across time and space but are culled by innovations that facilitate self-reliant production.     

Social intelligence in the spotted hyena (Crocuta crocuta)

If the large brains and great intelligence characteristic of primates were favoured by selection pressures associated with life in complex societies, then cognitive abilities and nervous systems with primate-like attributes should have evolved convergently in non-primate mammals living in large, elaborate societies in which social dexterity enhances individual fitness. The societies of spotted hyenas are remarkably like those of cercopithecine primates with respect to size, structure and patterns of competition and cooperation. These similarities set an ideal stage for comparative analysis of social intelligence and nervous system organization. As in cercopithecine primates, spotted hyenas use multiple sensory modalities to recognize their kin and other conspecifics as individuals, they recognize third-party kin and rank relationships among their clan mates, and they use this knowledge adaptively during social decision making. However, hyenas appear to rely more intensively than primates on social facilitation and simple rules of thumb in social decision making. No evidence to date suggests that hyenas are capable of true imitation. Finally, it appears that the gross anatomy of the brain in spotted hyenas might resemble that in primates with respect to expansion of frontal cortex, presumed to be involved in the mediation of social behaviour.     

Societal background influences social learning in cooperative decision making

Humans owe their ecological success to their great capacities for social learning and cooperation: learning from others helps individuals adjust to their environment and can promote cooperation in groups. Classic and recent studies indicate that the cultural organization of societies shapes the influence of social information on decision making and suggest that collectivist values (prioritizing the group relative to the individual) increase tendencies to conform to the majority. However, it is unknown whether and how societal background impacts social learning in cooperative interactions. Here we show that social learning in cooperative decision making systematically varies across two societies. We experimentally compare people's basic propensities for social learning in samples from a collectivist (China) and an individualist society (United Kingdom; total n?=?540) in a social dilemma and a coordination game. We demonstrate that Chinese participants base their cooperation decisions on information about their peers much more frequently than their British counterparts. Moreover, our results reveal remarkable societal differences in the type of peer information people consider. In contrast to the consensus view, Chinese participants tend to be substantially less majority-oriented than the British. While Chinese participants are inclined to adopt peer behavior that leads to higher payoffs, British participants tend to cooperate only if sufficiently many peers do so too. These results indicate that the basic processes underlying social transmission are not universal; rather, they vary with cultural conditions. As success-based learning is associated with selfish behavior and majority-based learning can help foster cooperation, our study suggests that in different societies social learning can play diverging roles in the emergence and maintenance of cooperation.     

Natural cooperators: Food sharing in humans and other primates

The study of cooperation is rich with theoretical models and laboratory experiments that have greatly advanced our knowledge of human uniqueness, but have sometimes lacked ecological validity. We therefore emphasize the need to tie discussions of human cooperation to the natural history of our species and its closest relatives, focusing on behavioral contexts best suited to reveal underlying selection pressures and evolved decision rules. 1 - 3 Food sharing is a fundamental form of cooperation that is well‐studied across primates and is particularly noteworthy because of its central role in shaping evolved human life history, social organization, and cooperative psychology. 1 - 16 Here we synthesize available evidence on food sharing in humans and other primates, tracing the origins of offspring provisioning, mutualism, trade, and reciprocity throughout the primate order. While primates may gain some benefits from sharing, humans, faced with more collective action problems in a risky foraging niche, expanded on primate patterns to buffer risk and recruit mates and allies through reciprocity and signaling, and established co‐evolving social norms of production and sharing. Differences in the necessity for sharing are reflected in differences in sharing psychology across species, thus helping to explain unique aspects of our evolved cooperative psychology.     

Marmoset monkeys evaluate third-party reciprocity

Many non-human primates have been observed to reciprocate and to understand reciprocity in one-to-one social exchanges. A recent study demonstrated that capuchin monkeys are sensitive to both third-party reciprocity and violation of reciprocity; however, whether this sensitivity is a function of general intelligence, evidenced by their larger brain size relative to other primates, remains unclear. We hypothesized that highly pro-social primates, even with a relatively smaller brain, would be sensitive to others'' reciprocity. Here, we show that common marmosets discriminated between human actors who reciprocated in social exchanges with others and those who did not. Monkeys accepted rewards less frequently from non-reciprocators than they did from reciprocators when the non-reciprocators had retained all food items, but they accepted rewards from both actors equally when they had observed reciprocal exchange between the actors. These results suggest that mechanisms to detect unfair reciprocity in third-party social exchanges do not require domain-general higher cognitive ability based on proportionally larger brains, but rather emerge from the cooperative and pro-social tendencies of species, and thereby suggest this ability evolved in multiple primate lineages.     

Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats

In cooperative animal societies, dominant females typically show higher breeding success than subordinates, and are commonly believed to control the extent of reproductive sharing. However, studies of social insect societies reveal that subordinates too can interfere with the breeding attempts of others, with important implications for the distribution of fitness within colonies. Here, we show that subordinate females in a high-skew vertebrate (the meerkat, Suricata suricatta), also exert a substantial influence over the reproductive attempts of others. In meerkat societies, pregnant dominants are known to kill subordinate litters, but we show that pregnant subordinates also kill pups; not only those of other subordinates but the dominant's as well. Litters born to females of any rank were half as likely to survive their first 4 days if a subordinate was pregnant. However, dominant females were more likely than subordinates to give birth when no other females were pregnant, and so lost fewer litters to infanticide than subordinates. This is probably due in part to dominants employing counter-tactics to reduce the incidence of subordinate pregnancy. We discuss the broad implications of subordinates having a degree of control over reproductive sharing for future attempts to understand the distribution of reproduction in animal societies.     

Hunting behavior of wild chimpanzees in the Taï National Park

Hunting is often considered one of the major behaviors that shaped early hominids' evolution, along with the shift toward a drier and more open habitat. We suggest that a precise comparison of the hunting behavior of a species closely related to man might help us understand which aspects of hunting could be affected by environmental conditions. The hunting behavior of wild chimpanzees is discussed, and new observations on a population living in the tropical rain forest of the Taï National Park, Ivory Coast, are presented. Some of the forest chimpanzees' hunting performances are similar to those of savanna-woodlands populations; others are different. Forest chimpanzees have a more specialized prey image, intentionally search for more adult prey, and hunt in larger groups and with a more elaborate cooperative level than savanna-woodlands chimpanzees. In addition, forest chimpanzees tend to share meat more actively and more frequently. These findings are related to some theories on aspects of hunting behavior in early hominids and discussed in order to understand some factors influencing the hunting behavior of wild chimpanzees. Finally, the hunting behavior of primates is compared with that of social carnivores.     

Different Responses to Reward Comparisons by Three Primate Species

Background

Recently, much attention has been paid to the role of cooperative breeding in the evolution of behavior. In many measures, cooperative breeders are more prosocial than non-cooperatively breeding species, including being more likely to actively share food. This is hypothesized to be due to selective pressures specific to the interdependency characteristic of cooperatively breeding species. Given the high costs of finding a new mate, it has been proposed that cooperative breeders, unlike primates that cooperate in other contexts, should not respond negatively to unequal outcomes between themselves and their partner. However, in this context such pressures may extend beyond cooperative breeders to other species with pair-bonding and bi-parental care.

Methods

Here we test the response of two New World primate species with different parental strategies to unequal outcomes in both individual and social contrast conditions. One species tested was a cooperative breeder (Callithrix spp.) and the second practiced bi-parental care (Aotus spp.). Additionally, to verify our procedure, we tested a third confamilial species that shows no such interdependence but does respond to individual (but not social) contrast (Saimiri spp.). We tested all three genera using an established inequity paradigm in which individuals in a pair took turns to gain rewards that sometimes differed from those of their partners.

Conclusions

None of the three species tested responded negatively to inequitable outcomes in this experimental context. Importantly, the Saimiri spp responded to individual contrast, as in earlier studies, validating our procedure. When these data are considered in relation to previous studies investigating responses to inequity in primates, they indicate that one aspect of cooperative breeding, pair-bonding or bi-parental care, may influence the evolution of these behaviors. These results emphasize the need to study a variety of species to gain insight in to how decision-making may vary across social structures.     

Regulation of neotenic differentiation through direct physical contact in the damp-wood termite Hodotermopsis sjostedti

Insectes Sociaux - In cooperative societies such as those of ants, honey bees, and termites, the number of reproductives is often regulated by social interactions. In many termite species, helper...     

Effects of social disruption in elephants persist decades after culling

Background

Multi-level fission-fusion societies, characteristic of a number of large brained mammal species including some primates, cetaceans and elephants, are among the most complex and cognitively demanding animal social systems. Many free-ranging populations of these highly social mammals already face severe human disturbance, which is set to accelerate with projected anthropogenic environmental change. Despite this, our understanding of how such disruption affects core aspects of social functioning is still very limited.

Results

We now use novel playback experiments to assess decision-making abilities integral to operating successfully within complex societies, and provide the first systematic evidence that fundamental social skills may be significantly impaired by anthropogenic disruption. African elephants (Loxodonta africana) that had experienced separation from family members and translocation during culling operations decades previously performed poorly on systematic tests of their social knowledge, failing to distinguish between callers on the basis of social familiarity. Moreover, elephants from the disrupted population showed no evidence of discriminating between callers when age-related cues simulated individuals on an increasing scale of social dominance, in sharp contrast to the undisturbed population where this core social ability was well developed.

Conclusions

Key decision-making abilities that are fundamental to living in complex societies could be significantly altered in the long-term through exposure to severely disruptive events (e.g. culling and translocation). There is an assumption that wildlife responds to increasing pressure from human societies only in terms of demography, however our study demonstrates that the effects may be considerably more pervasive. These findings highlight the potential long-term negative consequences of acute social disruption in cognitively advanced species that live in close-knit kin-based societies, and alter our perspective on the health and functioning of populations that have been subjected to anthropogenic disturbance.

     

How institutions shaped the last major evolutionary transition to large-scale human societies

What drove the transition from small-scale human societies centred on kinship and personal exchange, to large-scale societies comprising cooperation and division of labour among untold numbers of unrelated individuals? We propose that the unique human capacity to negotiate institutional rules that coordinate social actions was a key driver of this transition. By creating institutions, humans have been able to move from the default ‘Hobbesian’ rules of the ‘game of life’, determined by physical/environmental constraints, into self-created rules of social organization where cooperation can be individually advantageous even in large groups of unrelated individuals. Examples include rules of food sharing in hunter–gatherers, rules for the usage of irrigation systems in agriculturalists, property rights and systems for sharing reputation between mediaeval traders. Successful institutions create rules of interaction that are self-enforcing, providing direct benefits both to individuals that follow them, and to individuals that sanction rule breakers. Forming institutions requires shared intentionality, language and other cognitive abilities largely absent in other primates. We explain how cooperative breeding likely selected for these abilities early in the Homo lineage. This allowed anatomically modern humans to create institutions that transformed the self-reliance of our primate ancestors into the division of labour of large-scale human social organization.     

Diverse sensory cues for individual recognition

To be social, the ability to recognize and discriminate conspecific individuals is indispensable in social animals, including primates, rodents, birds, fish, and social insects which live in societies or groups. Recent studies using molecular biology, genetics, in vivo and in vitro physiology, and behavioral neuroscientific approaches have provided detailed insights into how animals process and recognize the information of individuals. Here, we review the most distinct sensory modalities for individual recognition in animals, namely, olfaction and vision. In the case of rodents, two polymorphic gene complexes have been identified in their urine as the key and essential pheromonal components for individual recognition: the major histocompatibility complex (MHC) and the major urinary protein (MUP). Animals flexibly utilize MHC and/or MUP, which are detected by the main olfactory epithelium (MOE) and/or the vomeronasal organ (VNO) for various types of social recognition, such as strain recognition, kin recognition, and individual recognition. In contrast, primates, including humans, primarily use facial appearance to identify others. Face recognition in humans and other animals is naturally unique from genetic, cognitive, developmental, and functional points of view. Importantly note that nurture effects during growth phase such as social experience and environment can also shape and tune this special cognitive ability, in order to distinguish subtle differences between individuals. In this review, we address such unique nature and nurture mechanisms for individual recognition.     

The evolution of cooperative breeding in birds: kinship,dispersal and life history

The evolution of cooperation among animals has posed a major problem for evolutionary biologists, and despite decades of research into avian cooperative breeding systems, many questions about the evolution of their societies remain unresolved. A review of the kin structure of avian societies shows that a large majority live in kin-based groups. This is consistent with the proposed evolutionary routes to cooperative breeding via delayed dispersal leading to family formation, or limited dispersal leading to kin neighbourhoods. Hypotheses proposed to explain the evolution of cooperative breeding systems have focused on the role of population viscosity, induced by ecological/demographic constraints or benefits of philopatry, in generating this kin structure. However, comparative analyses have failed to generate robust predictions about the nature of those constraints, nor differentiated between the viscosity of social and non-social populations, except at a coarse level. I consider deficiencies in our understanding of how avian dispersal strategies differ between social and non-social species, and suggest that research has focused too narrowly on population viscosity and that a broader perspective that encompasses life history and demographic processes may provide fresh insights into the evolution of avian societies.     

Social life: the paradox of multiple-queen colonies

The evolution of animal societies in which some individuals forego their own reproductive opportunities to help others to reproduce poses an evolutionary paradox that can be traced to Darwin. Altruism may evolve through kin selection when the donor and recipient of altruistic acts are related to each other, as generally is the case in social birds and mammals. Similarly, social insect workers are highly related to the brood they rear when colonies are headed by a single queen. However, recent studies have shown that insect colonies frequently contain several queens, with the effect of decreasing relatedness among colony members. How can one account for the origin and maintenance of such colonies? This evolutionary enigma presents many of the same theoretical challenges as does the evolution of cooperative breeding and eusociality.