Repression of competition favours cooperation: experimental evidence from bacteria

Repression of competition (RC) within social groups has been suggested as a key mechanism driving the evolution of cooperation, because it aligns the individual’s proximate interest with the interest of the group. Despite its enormous potential for explaining cooperation across all levels of biological organization, ranging from fair meiosis, to policing in insect societies, to sanctions in mutualistic interactions between species, there has been no direct experimental test of whether RC favours the spread of cooperators in a well‐mixed population with cheats. To address this, we carried out an experimental evolution study to test the effect of RC upon a cooperative trait – the production of iron‐scavenging siderophore molecules – in the bacterium Pseudomonas aeruginosa. We found that cooperation was favoured when competition between siderophore producers and nonsiderophore‐producing cheats was repressed, but not in a treatment where competition between the two strains was permitted. We further show that RC altered the cost of cooperation, but did not affect the relatedness among interacting individuals. This confirms that RC per se, as opposed to increased relatedness, has driven the observed increase in bacterial cooperation.     

Why acquiesce? Worker reproductive parasitism in the Eastern honeybee (Apis cerana)

Most societies are vulnerable to rogue individuals that pursue their own interests at the expense of the collective entity. Societies often protect themselves from selfish behaviour by ‘policing’, thereby enforcing the interests of the collective over those of individuals. In insect societies, for example, selfish workers can activate their ovaries and lay eggs, exploiting the collective brood rearing system for individual benefit. Policing, usually in the form of oophagy of worker‐laid eggs, controls selfish behaviour. Importantly, once an effective system of policing has evolved, the incentive for personal reproduction is lost, and ‘reproductive acquiescence’ in which ovary activation is rare or absent is predicted to evolve. Studies of social Hymenoptera have largely supported the prediction of worker ‘acquiescence’; workers of most species where policing is well developed have inactive ovaries. However, the eastern honeybee Apis cerana appears to be an exception. A. cerana colonies are characterized by highly efficient policing, yet about 5% of workers have active ovaries, even when a queen is present. This suggests that the evolution of acquiescence is incomplete in A. cerana. We regularly sampled male eggs and pupae from four A. cerana colonies. Workers had high levels of ovary activation overall (11.7%), and 3.8% of assignable male eggs and 1.1% of assignable male pupae were worker‐laid. We conclude that workers with active ovaries lay their eggs, but these rarely survive to pupation because of intense policing. We then used our findings as well as previously published data on A. cerana and A. mellifera to redo the meta‐analysis on which reproductive acquiescence theory is based. Including data on both species did not affect the relationship between effectiveness of policing and levels of worker reproduction. Their inclusion did, however, seriously weaken the relationship between relatedness among workers and levels of worker reproduction. Our work thus suggests that relatedness among workers does not affect the probability that workers will attempt to reproduce, but that it is coercion by peers that limits worker reproduction.     

Cheating can stabilize cooperation in mutualisms

Mutualisms present a challenge for evolutionary theory. How is cooperation maintained in the face of selection for selfishness and cheating? Both theory and data suggest that partner choice, where one species preferentially directs aid to the more cooperative members of the other species, is central to cooperation in many mutualisms. However, the theory has only so far considered the evolutionary effects of partner choice on one of the species in a mutualism in isolation. Here, we investigate the co-evolution of cooperation and choice in a choosy host and its symbiont. Our model reveals that even though choice and cooperation may be initially selected, it will often be unstable. This is because choice reduces variation in the symbiont and, therefore, tends to remove the selective incentive for its own maintenance (a scenario paralleled in the lek paradox in female choice and policing in within-species cooperation). However, we also show that when variability is reintroduced into symbionts each generation, in the form of less cooperative individuals, choice is maintained. This suggests that the presence of cheaters and cheater species in many mutualisms is central to the maintenance of partner choice and, paradoxically, cooperation itself.     

Bell miner provisioning calls are more similar among relatives and are used by helpers at the nest to bias their effort towards kin

Kin selection predicts that helpers in cooperative systems should preferentially aid relatives to maximize fitness. In family-based groups, this can be accomplished simply by assisting all group members. In more complex societies, where large numbers of kin and non-kin regularly interact, more sophisticated kin-recognition mechanisms are needed. Bell miners (Manorina melanophrys) are just such a system where individuals regularly interact with both kin and non-kin within large colonies. Despite this complexity, individual helpers of both sexes facultatively work harder when provisioning the young of closer genetic relatedness. We investigated the mechanism by which such adaptive discrimination occurs by assessing genetic kinship influences on the structure of more than 1900 provisioning vocalizations of 185 miners. These 'mew' calls showed a significant, positive linear increase in call similarity with increasing genetic relatedness, most especially in comparisons between male helpers and the breeding male. Furthermore, individual helping effort was more heavily influenced by call similarity to breeding males than to genetic relatedness, as predicted if call similarity is indeed the rule-of-thumb used to discriminate kin in this system. Individual mew call structure appeared to be inflexible and innate, providing an effective mechanism by which helpers can assess their relatedness to any individual. This provides, to our knowledge, the first example of a mechanism for fine-scale kin discrimination in a complex avian society.     

Limited food induces nepotism in drywood termites

The evolution of cooperation and altruistic behaviour where individuals forego their own reproduction to help others reproduce can be explained by kin selection. Depending on the costs and benefits provided, altruism can be evolutionarily favoured if it is directed at close relatives. A considerable body of data supports the role of relatedness as a key determinant of cooperation and conflict within societies. However, the role of ecological factors and, in particular, how these costs and benefits interact with relatedness remains poorly understood. By studying 16 colonies, here I show that in a drywood termite ecological factors determine the importance of relatedness. In colonies with limited food supply, nestmates restrict cooperative interactions mainly to close relatives, while non-discriminative cooperation occurs when food is abundant. This shows for the first time directly the interaction between ecological conditions and relatedness in shaping cooperation.     

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.     

Kin-informative recognition cues in ants

Although social groups are characterized by cooperation, they are also often the scene of conflict. In non-clonal systems, the reproductive interests of group members will differ and individuals may benefit by exploiting the cooperative efforts of other group members. However, such selfish behaviour is thought to be rare in one of the classic examples of cooperation--social insect colonies--because the colony-level costs of individual selfishness select against cues that would allow workers to recognize their closest relatives. In accord with this, previous studies of wasps and ants have found little or no kin information in recognition cues. Here, we test the hypothesis that social insects do not have kin-informative recognition cues by investigating the recognition cues and relatedness of workers from four colonies of the ant Acromyrmex octospinosus. Contrary to the theoretical prediction, we show that the cuticular hydrocarbons of ant workers in all four colonies are informative enough to allow full-sisters to be distinguished from half-sisters with a high accuracy. These results contradict the hypothesis of non-heritable recognition cues and suggest that there is more potential for within-colony conflicts in genetically diverse societies than previously thought.     

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.     

Konflikte und Konfliktlösung in den Staaten sozialer Insekten. Zwischen Superorganismus und Polizeistaat

Insect societies have traditionally been considered as harmonious, peaceful superorganisms in which all individuals altruistically cooperate to increase the reproductive success of the society as a whole. Over the last decade, this view has changed dramatically. Individual group members can pursue their egoistic interests at a cost to the whole society. The integrity of the society is sustained usually by the suppression of egoistic reproduction by workers, either through direct interference by the queen, the establishment of dominance hierarchies, or mutual policing and punishment. A detailed analysis of the processes in insect societies helps to understand which processes maintain the cooperation among egoistic individuals.     

Cooperation and the scale of competition in humans

Explaining cooperation is one of the greatest challenges for evolutionary biology. It is particularly a problem in species such as humans, where there is cooperation between nonrelatives. Numerous possible solutions have been suggested for the problem of cooperation between nonrelatives, including punishment, policing, and various forms of reciprocity. Here, we suggest that local competition for resources can pose a problem for these hypotheses, analogous to how it can select against cooperation between relatives. We extend the prisoner's dilemma (PD) game to show that local competition between interacting individuals can reduce selection for cooperation between nonrelatives. This is because, with local competition, fitness is relative to social partners, and cooperation benefits social partners. We then test whether nonrelated humans adjust their level of cooperation facultatively in response to the scale of competition when playing the PD for cash prizes. As predicted, we found that individuals were less likely to cooperate when competition was relatively local. Cooperation between humans will therefore be most likely when repeated interactions take place on a local scale between small numbers of people, and competition for resources takes place on a more global scale among large numbers of people.     

Cooperation‐mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.     

Costly punishment prevails in intergroup conflict

Understanding how societies resolve conflicts between individual and common interests remains one of the most fundamental issues across disciplines. The observation that humans readily incur costs to sanction uncooperative individuals without tangible individual benefits has attracted considerable attention as a proximate cause as to why cooperative behaviours might evolve. However, the proliferation of individually costly punishment has been difficult to explain. Several studies over the last decade employing experimental designs with isolated groups have found clear evidence that the costs of punishment often nullify the benefits of increased cooperation, rendering the strong human tendency to punish a thorny evolutionary puzzle. Here, we show that group competition enhances the effectiveness of punishment so that when groups are in direct competition, individuals belonging to a group with punishment opportunity prevail over individuals in a group without this opportunity. In addition to competitive superiority in between-group competition, punishment reduces within-group variation in success, creating circumstances that are highly favourable for the evolution of accompanying group-functional behaviours. We find that the individual willingness to engage in costly punishment increases with tightening competitive pressure between groups. Our results suggest the importance of intergroup conflict behind the emergence of costly punishment and human cooperation.     

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.     

Hunter–Gatherer population structure and the evolution of contingent cooperation

Unlike other vertebrates, humans cooperate in large groups with unrelated individuals. Many authors have argued that the evolution of such cooperation has resulted from reciprocity and other forms of contingent cooperation. This argument is not well supported by existing theory. The theory of contingent cooperation in pairs is well developed: reciprocating strategies are stable when common, and can increase when rare as long as population structure leads to modest levels of relatedness. In larger groups, however, it is not clear whether contingent cooperation can increase when rare. Existing work suggests that contingent strategies cannot increase unless relatedness is high, but depends on unrealistic assumptions about the effects of population structure. Here we develop and analyze a model incorporating a two level population structure that captures important features of human hunter–gatherer societies. This model suggests that previous work underestimates the range of conditions under which contingent cooperation can evolve, but also predicts that cooperation will not evolve unless (1) social groups are small, and (2) the relatedness within ethnolinguistic groups is at the high end of the range of empirical estimates.     

Cooperation and Competition Between Twins: Findings from a Prisoner’s Dilemma Game

Attention to factors influencing cooperation and competition during human social interaction has increased within recent years. This study tested the hypothesis that higher levels of cooperation would be associated with increased genetic relatedness between interactants, and explored questions concerning the expression of cooperative behavior over time. A Prisoner’s Dilemma game, in which participants elect to display cooperative, competitive, or exploitative behaviors relative to a partner, was administered to 59 monozygotic and 37 dizygotic twin pairs, between 10.92 and 82.67 years of age. Results from multivariate analysis of variance procedures, cross-lag sequential analyses, and hierarchical linear modeling supported associations between zygosity, and frequency and continuity of cooperation. Mechanisms by which zygosity may affect cooperation were explored by examining relationships between response combinations, and twins’ IQ similarity and social closeness. The findings are considered with reference to an evolutionary perspective on behavior that offers a theoretical basis for considering how the relative genetic relatedness of social partners affects their social-interactional processes and outcomes. This report is the first in a series of studies designed to address mechanisms underlying differences in cooperation among pairs who vary in average genetic commonality.     

Eider females form non-kin brood-rearing coalitions

Kin selection is a powerful tool for understanding cooperation among individuals, yet its role as the sole explanation of cooperative societies has recently been challenged on empirical grounds. These studies suggest that direct benefits of cooperation are often overlooked, and that partner choice may be a widespread mechanism of cooperation. Female eider ducks (Somateria mollissima) may rear broods alone, or they may pool their broods and share brood-rearing. Females are philopatric, and it has been suggested that colonies may largely consist of related females, which could promote interactions among relatives. Alternatively, shared brood care could be random with respect to relatedness, either because brood amalgamations are accidental and nonadaptive, or through group augmentation, assuming that the fitness of all group members increases with group size. We tested these alternatives by measuring the relatedness of co-tending eider females in enduring coalitions with microsatellite markers. Females formed enduring brood-rearing coalitions with each other at random with respect to relatedness. However, based on previous data, partner choice is nonrandom and dependent on female body condition. We discuss potential mechanisms underlying eider communal brood-rearing decisions, which may be driven by the specific ecological conditions under which sociality has evolved in this species.     

Sexual selection and reproductive success in hermaphroditic seabasses

Mating behavior in simultaneously hermaphroditic seabasses hasbeen often cited as an example of cooperation among unrelatedconspecifics. The predominant mating behavior in this groupinvolves egg trading, where individuals reciprocally fertilizeparcels of eggs from a partner. Egg trading has been suggestedas a good example of a tit-for-tat cooperative mating strategy.Although simultaneous hermaphroditic fishes are often held upas strong examples of cooperation in mating behavior, a closerexamination reveals significant sexual selection and sexualconflict between male and female roles among individuals. Inthe 7 species where data exist, there is a significant increasein male reproductive success with individual size, and in allbut 1 species success through male function increases fasterthan reproductive success through female function. Despite thismale-size advantage in simultaneous hermaphrodites, most speciesmaintain their hermaphroditism for their entire life, and theincreased male allocation while engaging in biased forms ofreciprocation appear to increase the evolutionary stabilityof hermaphroditism in these species. Thus, egg-trading behavioris probably more complicated than was initially recognized,with individuals releasing different numbers of eggs in spawns,spawning at different rates as males and females, and partitioningmale effort between pair and alternative mating tactics. Thedepartures from equal reciprocity can probably be best understoodby including aspects of traditional mating-system theory, withindividuals increasing male mating success through a varietyof behavioral tactics.     

Genetic structure of native ant supercolonies varies in space and time

Ant supercolonies are the largest cooperative units known in nature. They consist of networks of interconnected nests with hundreds of reproductive queens, where individuals move freely between nests, cooperate across nest boundaries and show little aggression towards non‐nestmates. The combination of high queen numbers and free mixing of workers, queens and brood between nests results in extremely low nestmate relatedness. In such low‐relatedness societies, cooperative worker behaviour appears maladaptive because it may aid random individuals instead of relatives. Here, we provide a comprehensive picture of genetic substructure in supercolonies of the native wood ant Formica aquilonia using traditional population genetic as well as network analysis methods. Specifically, we test for spatial and temporal variation in genetic structure of different classes of individuals within supercolonies and analyse the role of worker movement in determining supercolony genetic networks. We find that relatedness within supercolonies is low but positive when viewed on a population level, which may be due to limited dispersal of individuals and/or ecological factors such as nest site limitation and competition against conspecifics. Genetic structure of supercolonies varied with both sample class and sampling time point, which indicates that mobility of individuals varies according to both caste and season and suggests that generalizing has to be carried out with caution in studies of supercolonial species. Overall, our analysis provides novel evidence that native wood ant supercolonies exhibit fine‐scale genetic substructure, which may explain the maintenance of cooperation in these low‐relatedness societies.     

Escalated conflict in a social hierarchy

Animals that live in cooperative societies form hierarchies in which dominant individuals reap disproportionate benefits from group cooperation. The stability of these societies requires subordinates to accept their inferior status rather than engage in escalated conflict with dominants over rank. Applying the logic of animal contests to these cases predicts that escalated conflict is more likely where subordinates are reproductively suppressed, where group productivity is high, relatedness is low, and where subordinates are relatively strong. We tested these four predictions in the field on co-foundress associations of the paper wasp Polistes dominulus by inducing contests over dominance rank experimentally. Subordinates with lower levels of ovarian development, and those in larger, more productive groups, were more likely to escalate in conflict with their dominant, as predicted. Neither genetic relatedness nor relative body size had significant effects on the probability of escalation. The original dominant emerged as the winner in all except one escalated contest. The results provide the first evidence that reproductive suppression of subordinates increases the threat of escalated conflict, and hence that reproductive sharing can promote stability of the dominant-subordinate relationship.     

The evolution of cooperation by negotiation in a noisy world

Cooperative interactions among individuals are ubiquitous despite the possibility of exploitation by selfish free riders. One mechanism that may promote cooperation is ‘negotiation’: individuals altering their behaviour in response to the behaviour of others. Negotiating individuals decide their actions through a recursive process of reciprocal observation, thereby reducing the possibility of free riding. Evolutionary games with response rules have shown that infinitely many forms of the rule can be evolutionarily stable simultaneously, unless there is variation in individual quality. This potentially restricts the conditions under which negotiation could maintain cooperation. Organisms interact with one another in a noisy world in which cooperative effort and the assessment of effort may be subject to error. Here, we show that such noise can make the number of evolutionarily stable rules finite, even without quality variation, and so noise could help maintain cooperative behaviour. We show that the curvature of the benefit function is the key factor determining whether individuals invest more or less as their partner's investment increases, investing less when the benefit to investment has diminishing returns. If the benefits of low investment are very small then behavioural flexibility tends to promote cooperation, because negotiation enables cooperators to reach large benefits. Under some conditions, this leads to a repeating cycle in which cooperative behaviour rises and falls over time, which may explain between‐population differences in cooperative behaviour. In other conditions, negotiation leads to extremely high levels of cooperative behaviour, suggesting that behavioural flexibility could facilitate the evolution of eusociality in the absence of high relatedness.