Social structure, robustness, and policing cost in a cognitively sophisticated species

Conflict management is one of the primary requirements for social complexity. Of the many forms of conflict management, one of the rarest and most interesting is third-party policing, or intervening impartially to control conflict. Third-party policing should be hard to evolve because policers personally pay a cost for intervening, while the benefits are diffused over the whole group. In this study we investigate the incidence and costs of policing in a primate society. We report quantitative evidence of non-kin policing in the nonhuman primate, the pigtailed macaque. We find that policing is effective at reducing the intensity of or terminating conflict when performed by the most powerful individuals. We define a measure, social power consensus, that predicts effective low-cost interventions by powerful individuals and ineffective, relatively costly interventions by low-power individuals. Finally, we develop a simple probabilistic model to explore whether the degree to which policing can effectively reduce the societal cost of conflict is dependent on variance in the distribution of power. Our data and simple model suggest that third-party policing effectiveness and cost are dependent on power structure and might emerge only in societies with high variance in power.     

Resolving social conflict among females without overt aggression

Members of animal societies compete over resources and reproduction, but the extent to which such conflicts of interest are resolved peacefully (without recourse to costly or wasteful acts of aggression) varies widely. Here, we describe two theoretical mechanisms that can help to understand variation in the incidence of overt behavioural conflict: (i) destruction competition and (ii) the use of threats. The two mechanisms make different assumptions about the degree to which competitors are socially sensitive (responsive to real-time changes in the behaviour of their social partners). In each case, we discuss how the model assumptions relate to biological reality and highlight the genetic, ecological and informational factors that are likely to promote peaceful conflict resolution, drawing on empirical examples. We suggest that, relative to males, reproductive conflict among females may be more frequently resolved peacefully through threats of punishment, rather than overt acts of punishment, because (i) offspring are more costly to produce for females and (ii) reproduction is more difficult to conceal. The main need now is for empirical work to test whether the mechanisms described here can indeed explain how social conflict can be resolved without overt aggression.     

Reproductive skew theory unified: The general bordered tug-of-war model

Reproductive skew has been identified as a major dimension along which animal societies vary. Two major kinds of reproductive skew models are transactional models, which explain the distribution of reproduction within animal societies as the result of reproductive payments exchanged among group members with differential leverage, and tug-of-war models, in which the reproductive shares are determined by costly ‘tugs-of-war’. These two models have recently been synthesized to yield the mutual-pay, bordered tug-of-war model. In this paper, we extend the latter, show its evolutionary stability, and demonstrate that the generalized model yields four sub-models, namely the mutual-pay, alpha-pay, beta-pay, and pure tug-of-war. The alpha-pay sub-model turns out to closely resemble the original “concessions” transactional skew model, and the beta-pay sub-model turns out to have properties similar to the “restraint” transactional skew model. Thus, the general model unifies the four major models of reproductive skew and is rich in its predictions, as each sub-model exhibits different qualitative and quantitative relationships between reproductive skew or intra-group conflict and the ecological and genetic factors that determine skew and conflict. The conditions favoring transitions among these sub-models also are precisely predicted by the general model. The general model accommodates data from acorn woodpeckers and primitively eusocial bees potentially can account for many of the highly varied empirical findings on reproductive skew. We suggest further research that focuses on (1) determining which model is suitable for certain species and (2) understanding why and how various social animals resolve their breeding conflict by different conflict resolution mechanisms.     

Policing and punishment across the domains of social evolution

Several decades of research in humans, other vertebrates, and social insects have offered fascinating insights into the dynamics of punishment (and its subset, policing), but authors have only rarely addressed whether there are fundamental joint principles underlying the maintenance of these behaviors. Here we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punishing roles in animal societies. We apply our scheme to societies of eusocial Hymenoptera and nonhuman vertebrate social breeders, and we outline potential extensions for understanding conflict regulation among cells in metazoan bodies and unrelated individuals in human societies. We highlight that: 1) no social unit is expected to express punishment behavior unless it collects positive inclusive fitness benefits that surpass alternative benefits of bystanding; 2) punishment with public good benefits can be maintained through either direct fitness benefits (coercion) or indirect fitness benefits (correction) or both; 3) differences across social systems in the distributions of power, relatedness, and reproductive options drive variation in the extent to which individuals actively punish; and 4) inclusive fitness logic captures many punishment‐relevant evolutionary and ecological variables in a single framework that appears to apply across very different types of social arrangements. Synthesis Researchers have long observed that individuals in animal societies punish (and by extension, police) each other, but they have rarely investigated whether general principles underlie this behavior across social arrangements. In this paper, we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punisher roles in animal societies. We apply the approach to eusocial insects and cooperatively breeding vertebrates and outline extensions towards the control of cancer cell lineages and punishment in human groups. We highlight how variation in specific social variables may drive differences in punishing/policing across the social domains.     

Colony size,social complexity and reproductive conflict in social insects

The broad limits of mature colony size in social insect species are likely to be set by ecological factors. However, any change in colony size has a number of important social consequences. The most fundamental is a change in the expected reproductive potential of workers. If colony size rises, workers experience a fall in their chances of becoming replacement reproductives and, it is shown, increasing selection for mutual inhibition of one another's reproduction (worker policing). As workers’ reproductive potential falls, the degree of dimorphism between reproductive and worker castes (morphological skew) can rise. This helps explain why small societies have low morphological skew and tend to be simple in organization, whereas large societies have high morphological skew and tend to be complex. The social consequences of change in colony size may also alter colony size itself in a process of positive feedback. For these reasons, small societies should be characterized by intense, direct conflict over reproduction and caste determination. By contrast, conflict in large societies should predominantly be over brood composition, and members of these societies should be relatively compliant to manipulation of their caste. Colony size therefore deserves fuller recognition as a key determinant, along with kin structure, of social complexity, the reproductive potential of helpers, the degree of caste differentiation, and the nature of within-group conflict.     

The threat of punishment enforces peaceful cooperation and stabilizes queues in a coral-reef fish

Social queues, in which subordinates wait for their turn to inherit dominant breeding status, are a familiar feature of many animal societies. However, little is known about the mechanisms stabilizing social queues given the inevitable conflict over rank between group members. Here, we report the role of punishment and cooperation in promoting the stability of size-based queues in a coral-dwelling goby, Paragobiodon xanthosomus (Gobiidae). Quantitative analysis of the size-structure of queues revealed that individuals of adjacent rank differ in size by a specific size ratio, and comparisons of individual growth rates within queues demonstrated that specific size ratios are maintained over time via the regulation of subordinate growth rates. Furthermore, contest experiments demonstrated that the specific size ratio represents a threshold above which the subordinates become a threat to their immediate dominant, and as a result, dominants evict subordinates that exceed this size ratio from the group. We propose that threshold size ratios are maintained by subordinates as a form of peaceful cooperation whereby they avoid inflicting costs on dominants, and that such cooperation arises in response to the threat of punishment in the form of eviction by dominants. Societal stability is therefore achieved through the effects of punishment and cooperation acting in concert to promote the resolution of conflict over rank between group members.     

Suppression of social conflict and evolutionary transitions to cooperation

Evolutionary conflict arises at all levels of biological organization and presents a barrier to the evolution of cooperation. This barrier can be overcome by mechanisms that reduce the disparity between the fitness optima of subunits, sometimes called the "battleground" of conflict. An alternative, unstudied possibility is that effort invested in conflict is unprofitable. This possibility has received little attention because most existing models of social conflict assume that fitness depends on the ratio of players' conflict efforts, so that "peaceful" outcomes featuring zero conflict effort are evolutionarily unstable. Here I show that peaceful outcomes are stable where success depends on the difference rather than the ratio of efforts invested in conflict. These difference form models are particularly appropriate to model strategies of suppression or policing. The model suggests that incomplete information and asymmetries in strength can act to eliminate costly conflict within groups, even among unrelated individuals, and thereby facilitate the evolution of cooperation.     

Family feuds: social competition and sexual conflict in complex societies

Darwin was initially puzzled by the processes that led to ornamentation in males-what he termed sexual selection-and those that led to extreme cooperation and altruism in complex animal societies-what was later termed kin selection. Here, I explore the relationships between sexual and kin selection theory by examining how social competition for reproductive opportunities-particularly in females-and sexual conflict over mating partners are inherent and critical parts of complex altruistic societies. I argue that (i) patterns of reproductive sharing within complex societies can drive levels of social competition and reproductive conflict not only in males but also in females living in social groups, and ultimately the evolution of female traits such as ornaments and armaments; (ii) mating conflict over female choice of sexual partners can influence kin structure within groups and drive the evolution of complex societies; and (iii) patterns of reproductive sharing and conflict among females may also drive the evolution of complex societies by influencing kin structure within groups. Ultimately, complex societies exhibiting altruistic behaviour appear to have only arisen in taxa where social competition over reproductive opportunities and sexual conflict over mating partners were low. Once such societies evolved, there were important selective feedbacks on traits used to regulate and mediate intra-sexual competition over reproductive opportunities, particularly in females.     

Dominance hierarchies reduce the number of hopeful reproductives in polygynous queenless ants

Summary. In many animal societies aggressive interactions regulate essential features such as feeding order and reproductive rights. Because aggressive interactions are costly the number of individuals competing for direct reproduction (hopeful reproductives) affects colony productivity. Using mathematical models, based on the costs/benefits trade-off for a worker to attempt to become a reproductive, we determine the number of hopeful reproductives expected to occur in insect societies with totipotent workers and several reproductives. The model is based on the biology of the polygynous queenless ant Rhytidoponera confusa (Formicidae: Ectatomminae), where every worker can potentially reproduce but only a few actually do, but is valid for all societies with totipotent individuals. We compare the number of hopeful reproductives predicted in the absence of a dominance hierarchy and with a linear dominance hierarchy, and we investigate the effects of colony size, relatedness, and mortality. The models show that a linear dominance hierarchy reduces the number of hopeful reproductives, and additional unpublished models show that this reduction is lower in non-linear hierarchies. Dominance hierarchies are thus favoured by natural selection. Larger colony size and higher mortalities result in longer hierarchy, whereas higher relatedness shortens hierarchy length. These predictions were successfully tested with eight colonies of R. confusa.Received 2 August 2004; revised 10 January 2005; accepted 12 January 2005.     

Grooming coercion and the post-conflict trading of social services in wild Barbary macaques

In animal and human societies, social services such as protection from predators are often exchanged between group members. The tactics that individuals display to obtain a service depend on its value and on differences between individuals in their capacity to aggressively obtain it. Here we analysed the exchange of valuable social services (i.e. grooming and relationship repair) in the aftermath of a conflict, in wild Barbary macaques (Macaca sylvanus). The relationship repair function of post-conflict affiliation (i.e. reconciliation) was apparent in the victim but not in the aggressor. Conversely, we found evidence for grooming coercion by the aggressor; when the victim failed to give grooming soon after a conflict they received renewed aggression from the aggressor. We argue that post-conflict affiliation between former opponents can be better described as a trading of social services rather than coercion alone, as both animals obtain some benefits (i.e. grooming for the aggressor and relationship repair for the victim). Our study is the first to test the importance of social coercion in the aftermath of a conflict. Differences in competitive abilities can affect the exchange of services and the occurrence of social coercion in animal societies. This may also help explain the variance between populations and species in their social behaviour and conflict management strategies.     

Detecting instability in animal social networks: genetic fragmentation is associated with social instability in rhesus macaques

The persistence of biological systems requires evolved mechanisms which promote stability. Cohesive primate social groups are one example of stable biological systems, which persist in spite of regular conflict. We suggest that genetic relatedness and its associated kinship structure are a potential source of stability in primate social groups as kinship structure is an important organizing principle in many animal societies. We investigated the effect of average genetic relatedness per matrilineal family on the stability of matrilineal grooming and agonistic interactions in 48 matrilines from seven captive groups of rhesus macaques. Matrilines with low average genetic relatedness show increased family-level instability such as: more sub-grouping in their matrilineal groom network, more frequent fighting with kin, and higher rates of wounding. Family-level instability in multiple matrilines within a group is further associated with group-level instability such as increased wounding. Stability appears to arise from the presence of clear matrilineal structure in the rhesus macaque group hierarchy, which is derived from cohesion among kin in their affiliative and agonistic interactions with each other. We conclude that genetic relatedness and kinship structure are an important source of group stability in animal societies, particularly when dominance and/or affilative interactions are typically governed by kinship.     

A Transactional Theory of Within-Group Conflict

Transactional models of social evolution emphasize that dominant members of the society can be favored to donate parcels of reproduction to subordinate members in return for cooperation. I construct a formal theory of intragroup conflict within the framework of transactional models by determining the maximum extent to which colony members can be selfish without destabilizing the group. The difference between the maximum value of the subordinate's fraction of group reproduction that the dominant can tolerate before ejecting the subordinate and the minimum value required by the subordinate to stay and cooperate peacefully in the group defines the "window of selfishness," which in turn predicts the frequency of within-group conflict. The window of selfishness tends to increase with increasing group reproductive output, increasingly harsh ecological constraints on solitary breeding, and, counterintuitively, increasing relatedness between subordinate and dominant. Increasing fighting ability of the subordinate can either widen or narrow the window of selfishness, the latter being most likely when ecological constraints on group living are strong. Although increasing relatedness is predicted to increase the rate of within-group aggression, the mean intensity of an aggressive act should decline, as predicted by the general theory of honest signaling between relatives and the tug-of-war models of within-group selfishness. In the bidding game, in which multiple dominants bid for the services of a subordinate, the window of selfishness is predicted to have zero width. A zero-width window of selfishness and low conflict also are predicted for saturated N-person groups, that is, groups whose total output is a concave function of group size and in which the dominant is not favored to admit additional subordinates. The model's predictions are compared to empirical evidence and to predictions of alternative models of intragroup aggression, including the value-aggression model and the pure tug-of-war model.     

Reproductive competition triggers mass eviction in cooperative banded mongooses

In many vertebrate societies, forced eviction of group members is an important determinant of population structure, but little is known about what triggers eviction. Three main explanations are: (i) the reproductive competition hypothesis, (ii) the coercion of cooperation hypothesis, and (iii) the adaptive forced dispersal hypothesis. The last hypothesis proposes that dominant individuals use eviction as an adaptive strategy to propagate copies of their alleles through a highly structured population. We tested these hypotheses as explanations for eviction in cooperatively breeding banded mongooses (Mungos mungo), using a 16-year dataset on life history, behaviour and relatedness. In this species, groups of females, or mixed-sex groups, are periodically evicted en masse. Our evidence suggests that reproductive competition is the main ultimate trigger for eviction for both sexes. We find little evidence that mass eviction is used to coerce helping, or as a mechanism to force dispersal of relatives into the population. Eviction of females changes the landscape of reproductive competition for remaining males, which may explain why males are evicted alongside females. Our results show that the consequences of resolving within-group conflict resonate through groups and populations to affect population structure, with important implications for social evolution.     

The function of peaceful post-conflict contacts among primates

Reconciliation has been the subject of considerable research in the last decade, and researchers have demonstrated that in many species of Old World monkeys and apes former opponents are more likely to engage in friendly interactions in the minutes that follow conflicts than they are at other times.de Waal has suggested that the function of these interactions is to mend relationships that have been damaged by conflict. Although peaceful post-conflict interactions are thought to have long-term effects upon the nature of social relationships, behavioral evidence presently indicates that the effects of these interactions may be limited to the post-conflict period. Theoretical considerations also raise some doubts about whether the relationship-repair hypothesis is cogent. Data that demonstrate that peaceful post-conflict interactions facilitate peaceful interactions and relieve victim's uncertainty and anxiety about whether conflict will be continued suggest that peaceful post-conflict interactions may be a means to reestablish contact with former opponents. Thus, they appear to function as predictive signals that the actor is going to stop fighting and behave peacefully. Such signals may be important in a broad range of social contexts.     

Reputation and the evolution of conflict

The outcomes of conflicts in many human societies generate reputation effects that influence the nature of later conflicts. Those willing to escalate over even trivial offenses are considered honorable whereas those who do not are considered dishonorable (Nisbett & Cohen, 1996). Here I extend Maynard Smith's hawk-dove model of animal conflict to explore the logic of a strategy which uses reputation about its opponents to regulate its behavior. I show that a reputation-based strategy does well when (1) the value of the resource is large relative to the cost of losing a fight, (2) communities are stable, and (3) reputations are well known but subject to some amount of error. Reputation-based strategies may thus result in greater willingness to fight, but less fighting at equilibrium, depending upon the nature of the contests and the local socioecology. Additionally, this strategy is robust in the presence of poor knowledge about reputation.     

Complex societies

The complexity of human societies of the past few thousand years rivals that of social insect societies. We hypothesize that two sets of social “instincts” underpin and constrain the evolution of complex societies. One set is ancient and shared with other social primate species, and one is derived and unique to our lineage. The latter evolved by the late Pleistocene, and led to the evolution of institutions of intermediate complexity in acephalous societies. The institutions of complex societies often conflict with our social instincts. The complex societies of the past few thousand years can function only because cultural evolution has created effective “work-arounds” to manage such instincts. We describe a series of work-arounds and use the data on the relative effectiveness of WWII armies to test the work-around hypothesis. Richerson received his Ph.D. degree in zoology from UC Davis in 1969. He is currently a professor in the Department of Environmental Science and Policy. In addition to his work in cultural evolution, he has worked on the limnology of Lake Tahoe and Clear Lake in California, and on Lake Titicaca in Peru and Bolivia. Boyd received his Ph.D. degree in ecology from UC Davis in 1975, though his thesis work was a resource economics problem. He is currently a professor of anthropology at UCLA. His research interests besides cultural evolution are game theory and a small bit of primatology from time to time.     

Adaptation and the genetics of social behaviour

In recent years much progress has been made towards understanding the selective forces involved in the evolution of social behaviour including conflicts over reproduction among group members. Here, I argue that an important additional step necessary for advancing our understanding of the resolution of potential conflicts within insect societies is to consider the genetics of the behaviours involved. First, I discuss how epigenetic modifications of behaviour may affect conflict resolution within groups. Second, I review known natural polymorphisms of social organization to demonstrate that a lack of consideration of the genetic mechanisms involved may lead to erroneous explanations of the adaptive significance of behaviour. Third, I suggest that, on the basis of recent genetic studies of sexual conflict in Drosophila, it is necessary to reconsider the possibility of within-group manipulation by means of chemical substances (i.e. pheromones). Fourth, I address the issue of direct versus indirect genetic effects, which is of particular importance for the study of behaviour in social groups. Fifth, I discuss the issue of how a genetic influence on dominance hierarchies and reproductive division of labour can have secondary effects, for example in the evolution of promiscuity. Finally, because the same sets of genes (e.g. those implicated in chemical signalling and the responses that are triggered) may be used even in species as divergent as ants, cooperative breeding birds and primates, an integration of genetic mechanisms into the field of social evolution may also provide unifying ideas.     

Long-term memory of individual identity in ant queens

Remembering individual identities is part of our own everyday social life. Surprisingly, this ability has recently been shown in two social insects. While paper wasps recognize each other individually through their facial markings, the ant, Pachycondyla villosa, uses chemical cues. In both species, individual recognition is adaptive since it facilitates the maintenance of stable dominance hierarchies among individuals, and thus reduces the cost of conflict within these small societies. Here, we investigated individual recognition in Pachycondyla ants by quantifying the level of aggression between pairs of familiar or unfamiliar queens over time. We show that unrelated founding queens of P. villosa and Pachycondyla inversa store information on the individual identity of other queens and can retrieve it from memory after 24h of separation. Thus, we have documented for the first time that long-term memory of individual identity is present and functional in ants. This novel finding represents an advance in our understanding of the mechanism determining the evolution of cooperation among unrelated individuals.     

The role of threats in animal cooperation

In human societies, social behaviour is strongly influenced by threats of punishment, even though the threats themselves rarely need to be exercised. Recent experimental evidence suggests that similar hidden threats can promote cooperation and limit within-group selfishness in some animal systems. In other animals, however, threats appear to be ineffective. Here I review theoretical and empirical studies that help to understand the evolutionary causes of these contrasting patterns, and identify three factors—impact, accuracy and perception—that together determine the effectiveness of threats to induce cooperation.     

Exploring the components, asymmetry and distribution of relationship quality in wild Barbary macaques (Macaca sylvanus)

Social relationships between group members are a key feature of many animal societies. The quality of social relationships has been described by three main components: value, compatibility and security, based on the benefits, tenure and stability of social exchanges. We aimed to analyse whether this three component structure could be used to describe the quality of social relationships in wild Barbary macaques (Macaca sylvanus). Moreover, we examined whether relationship quality was affected by the sex, age and rank differences between social partners, and investigated the asymmetric nature of social relationships. We collected over 1,900 hours of focal data on seven behavioural variables measuring relationship quality, and used principal component analysis to investigate how these variables clustered together. We found that relationship quality in wild Barbary macaques can be described by a three component structure that represents the value, compatibility and security of a relationship. Female-female dyads had more valuable relationships and same-age dyads more compatible relationships than any other dyad. Rank difference had no effect on the quality of a social relationship. Finally, we found a high degree of asymmetry in how members of a dyad exchange social behaviour. We argue that the asymmetry of social relationships should be taken into account when exploring the pattern and function of social behaviour in animal societies.