The co-evolution of individual behaviors and social institutions

We present agent-based simulations of a model of a deme-structured population in which group differences in social institutions are culturally transmitted and individual behaviors are genetically transmitted. We use a standard extended fitness accounting framework to identify the parameter space for which this co-evolutionary process generates high levels of group-beneficial behaviors. We show that intergroup conflicts may explain the evolutionary success of both: (a) altruistic forms of human sociality towards unrelated members of one's group; and (b) group-level institutional structures such as food sharing which have emerged and diffused repeatedly in a wide variety of ecologies during the course of human history. Group-beneficial behaviors may evolve if (a) they inflict sufficient fitness costs on outgroup individuals and (b) group-level institutions limit the individual fitness costs of these behaviors and thereby attenuate within-group selection against these behaviors. Thus, the evolutionary success of individually costly but group-beneficial behaviors in the relevant environments during the first 90,000 years of anatomically modern human existence may have been a consequence of distinctive human capacities in social institution building.     

Conditions for the evolution of altruism under darwinian selection

A model of population structure is discussed which under certain circumstances allows for evolution of altruistic traits, beyond the classical restrictions imposed by kin selection theory and related concepts such as reciprocal altruism. Essentially, the model sees a large population as socially subdivided into small groups without any barriers, however, to free random mating. An altruistic trait is defined as lowering, locally, the fitness of a carrier below that of noncarriers within the same group; but the local fitness of an individual randomly chosen in a group increases with the number of altruists. It is shown that altruism can evolve even if the groups are randomly formed. The conditions for such evolution are contrasted with those prevailing when the groups are formed either with some phenotypic assortment between the members or on the basis of kinship. It is shown that any possibility of evolution tends to rapidly disappear as groups become large, unless there is complete positive assortment or individuals in the groups are kin. The example of alarm calls is also considered, and the two extremes of random and sib-groups are contrasted, using a model by Maynard Smith. It is shown that alarm calls can evolve in small groups of unrelated individuals under conditions qualitatively similar but quantitatively more rigorous than those prevailing for sib-groups.     

The cost of conflict in aphid societies

Most social aphids are found within plant galls, inside of which clonally‐derived family groups feed, and specialized larval castes forego reproduction and perform various cooperative tasks, including group defence. When unrelated aphids move between clones, conditions are ripe for conflict because galls and cooperative defence are shared resources that are vulnerable to exploitation. A key unknown is whether conflict is costly in aphid social groups. We show that diversity within groups is negatively correlated with performance in the North American social aphid, Pemphigus obesinymphae. A substantial fraction of productivity is invested into drifting. However, drifting aphids tend to mature and depart non‐natal galls prior to the seasonal peak in fecundity. These results suggest that when unrelated individuals move between groups, social aphids may experience conditions consistent with a tragedy of the commons. These results also emphasize the strongly convergent properties associated with conflict across the spectrum of animal and microbial sociality.     

An evolutionary analysis of the relationship between spite and altruism

We investigate the selective pressures on a social trait when evolution occurs in a population of constant size. We show that any social trait that is spiteful simultaneously qualifies as altruistic. In other words, any trait that reduces the fitness of less related individuals necessarily increases that of related ones. Our analysis demonstrates that the distinction between "Hamiltonian spite" and "Wilsonian spite" is not justified on the basis of fitness effects. We illustrate this general result with an explicit model for the evolution of a social act that reduces the recipient's survival ("harming trait"). This model shows that the evolution of harming is favoured if local demes are of small size and migration is low (philopatry). Further, deme size and migration rate determine whether harming evolves as a selfish strategy by increasing the fitness of the actor, or as a spiteful/altruistic strategy through its positive effect on the fitness of close kin.     

Inbreeding and evolution by kin selection

Because alleles associated with altruistic behaviors can increase in frequency when altruists increase the fitness of closely related individuals, it has been assumed that inbreeding presents the most favorable conditions for the evolution of altruism. Using a family-structured model of kin selection, we varied the proportion of the population mating with sibs and the proportion mating randomly to investigate the hypothesis that inbreeding facilitates the evolution of altruistic behaviors.We partitioned total gene frequency change of the altruistic allele into two components: (1) the change in gene frequency owing to selection within families, or individual selection; this component of selection is always negative and selects against altruistic social behaviors; and (2) the change in gene frequency owing to fitness differences between families, or group selection; this component of selection favors the evolution of altruistic social behaviors. Because inbreeding increases the component of group selection at the expense of individual selection by increasing the between-group variation, it facilitates the spread of the altruistic allele. Computer simulations show that even small amounts of inbreeding (within-sibship mating) significantly increase the rate of gene frequency change.     

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.     

‘Adoption’ by Maternal Siblings in Wild Chimpanzees

The adoption of unrelated orphaned infants is something chimpanzees and humans have in common. Providing parental care has fitness implications for both the adopter and orphan, and cases of adoption have thus been cited as evidence for a shared origin of an altruistic behaviour. We provide new data on adoptions in the free-living Sonso chimpanzee community in Uganda, together with an analysis of published data from other long-term field sites. As a default pattern, we find that orphan chimpanzees do not become adopted by adult group members but wherever possible associate with each other, usually as maternal sibling pairs. This occurs even if both partners are still immature, with older individuals effectively becoming ‘child household heads’. Adoption of orphans by unrelated individuals does occur but usually only if no maternal siblings or other relatives are present and only after significant delays. In conclusion, following the loss of their mother, orphaned chimpanzees preferentially associate along pre-existing social bonds, which are typically strongest amongst maternal siblings.     

Cooperation between non-relatives in a primitively eusocial paper wasp,Polistes dominula

In cooperatively breeding vertebrates, the existence of individuals that help to raise the offspring of non-relatives is well established, but unrelated helpers are less well known in the social insects. Eusocial insect groups overwhelmingly consist of close relatives, so populations where unrelated helpers are common are intriguing. Here, we focus on Polistes dominula—the best-studied primitively eusocial wasp, and a species in which nesting with non-relatives is not only present but frequent. We address two major questions: why individuals should choose to nest with non-relatives, and why such individuals participate in the costly rearing of unrelated offspring. Polistes dominula foundresses produce more offspring of their own as subordinates than when they nest independently, providing a potential explanation for co-founding by non-relatives. There is some evidence that unrelated subordinates tailor their behaviour towards direct fitness, while the role of recognition errors in generating unrelated co-foundresses is less clear. Remarkably, the remote but potentially highly rewarding chance of inheriting the dominant position appears to strongly influence behaviour, suggesting that primitively eusocial insects may have much more in common with their social vertebrate counterparts than has commonly been thought.     

GROUP FORMATION AND THE EVOLUTION OF SOCIALITY

In spite of its intrinsic evolutionary instability, altruistic behavior in social groups is widespread in nature, spanning from organisms endowed with complex cognitive abilities to microbial populations. In this study, we show that if social individuals have an enhanced tendency to form groups and fitness increases with group cohesion, sociality can evolve and be maintained in the absence of actively assortative mechanisms such as kin recognition or nepotism toward other carriers of the social gene. When explicitly taken into account in a game‐theoretical framework, the process of group formation qualitatively changes the evolutionary dynamics with respect to games played in groups of constant size and equal grouping tendencies. The evolutionary consequences of the rules underpinning the group size distribution are discussed for a simple model of microbial aggregation by differential attachment, indicating a way to the evolution of sociality bereft of peer recognition.     

"Runaway" social evolution: reinforcing selection for inbreeding and altruism.

Kin selection theory predicts that altruistic behaviors, those that decrease the fitness of the individual performing the behavior but increase the fitness of the recipient, can increase in frequency if the individuals interacting are closely related. Several studies have shown that inbreeding therefore generally increases the effectiveness of kin selection when fitnesses are linear, additive functions of the number of altruists in the family, although with extreme forms of altruism, inbreeding can actually retard the evolution of altruism. These models assume that a constant proportion of the population mates at random and a constant proportion practices some form of inbreeding. In order to investigate the effect of inbreeding on the evolution of altruistic behavior when the mating structure is allowed to evolve, we examined a two-locus model by computer simulation of a diploid case and illustrated the important qualitative features by mathematical analysis of a haploid case. One locus determines an individual's propensity to perform altruistic social behavior and the second locus determines the probability that an individual will mate within its sibship. We assumed positive selection for altruism and no direct selection at the inbreeding locus. We observed that the altruistic allele and the inbreeding allele become positively associated, even when the initial conditions of the model assume independence between these loci. This linkage disequilibrium becomes established, because the altruistic allele increases more rapidly in the inbreeding segment of the population. This association subsequently results in indirect selection on the inbreeding locus. However, the dynamics of this model go beyond a simple "hitch-hiking" effect, because high levels of altruism lead to increased inbreeding, and high degrees of inbreeding accelerate the rate of change of the altruistic allele in the entire population. Thus, the dynamics of this model are similar to those of "runaway" sexual selection, with gene frequency change at the two loci interactively causing rapid evolutionary change.     

Kin Associations during Nest Founding in an Allodapine Bee Exoneura robusta: do Females Distinguish between Relatives and Familiar Nestmates?

True recognition of kin can have important fitness consequences in terms of directing altruistic behaviours toward close relatives (nepotism) and avoiding inbreeding. However, recent evidence suggests that some social insect species cannot or do not distinguish their closest relatives from among nestmates in important fitness-based contexts. Such findings are relevant to kin selection theories where individuals are expected to preferentially rear close relatives in order to gain inclusive fitness benefits. Here, allozyme markers are used to examine whether female Exoneura robusta individuals preferentially nest with their closest kin when given a choice of familiar previous nestmates. The results suggest these bees do not prefer kin over non-kin nestmates. Kin associations during nest founding in this species are probably due to philopatry and/or association with previously familiar nestmates.     

Social competition or correlated strategy?

Summary Cooperation need not be expressed identically among individuals in a group to enhance the fitness of all. Complementary tasks can be allocated differentially, with task assignment differentially affecting individual absolute fitness. Such differential task assignment is often considered a consequence of social competition to avoid fitness-limiting tasks. I suggest an alternative, evoking an area of evolutionary game theory often overlooked in analyses of cooperation, where task assignment can be fundamentally arbitrary relative to competitive ability. Dominance, implied, ritual or actual, need not be a consequence of social competition for resources within groups.     

Charitable giving as a signal of trustworthiness: Disentangling the signaling benefits of altruistic acts

It has been shown that psychological predispositions to benefit others can motivate human cooperation and the evolution of such social preferences can be explained with kin or multi-level selection models. It has also been shown that cooperation can evolve as a costly signal of an unobservable quality that makes a person more attractive with regard to other types of social interactions. Here we show that if a proportion of individuals with social preferences is maintained in the population through kin or multi-level selection, cooperative acts that are truly altruistic can be a costly signal of social preferences and make altruistic individuals more trustworthy interaction partners in social exchange. In a computerized laboratory experiment, we test whether altruistic behavior in the form of charitable giving is indeed correlated with trustworthiness and whether a charitable donation increases the observing agents' trust in the donor. Our results support these hypotheses and show that, apart from trust, responses to altruistic acts can have a rewarding or outcome-equalizing purpose. Our findings corroborate that the signaling benefits of altruistic acts that accrue in social exchange can ease the conditions for the evolution of social preferences.     

Evolution of indirect reciprocity by social information: the role of trust and reputation in evolution of altruism

The complexity of human's cooperative behavior cannot be fully explained by theories of kin selection and group selection. If reciprocal altruism is to provide an explanation for altruistic behavior, it would have to depart from direct reciprocity, which requires dyads of individuals to interact repeatedly. For indirect reciprocity to rationalize cooperation among genetically unrelated or even culturally dissimilar individuals, information about the reputation of individuals must be assessed and propagated in a population. Here, we propose a new framework for the evolution of indirect reciprocity by social information: information selectively retrieved from and propagated through dynamically evolving networks of friends and acquaintances. We show that for indirect reciprocity to be evolutionarily stable, the differential probability of trusting and helping a reputable individual over a disreputable individual, at a point in time, must exceed the cost-to-benefit ratio of the altruistic act. In other words, the benefit received by the trustworthy must out-weigh the cost of helping the untrustworthy.     

Leadership in elephants: the adaptive value of age

The value of age is well recognized in human societies, where older individuals often emerge as leaders in tasks requiring specialized knowledge, but what part do such individuals play in other social species? Despite growing interest in how effective leadership might be achieved in animal social systems, the specific role that older leaders may play in decision-making has rarely been experimentally investigated. Here, we use a novel playback paradigm to demonstrate that in African elephants (Loxodonta africana), age affects the ability of matriarchs to make ecologically relevant decisions in a domain critical to survival—the assessment of predatory threat. While groups consistently adjust their defensive behaviour to the greater threat of three roaring lions versus one, families with younger matriarchs typically under-react to roars from male lions despite the severe danger they represent. Sensitivity to this key threat increases with matriarch age and is greatest for the oldest matriarchs, who are likely to have accumulated the most experience. Our study provides the first empirical evidence that individuals within a social group may derive significant benefits from the influence of an older leader because of their enhanced ability to make crucial decisions about predatory threat, generating important insights into selection for longevity in cognitively advanced social mammals.     

Why do Hymenopteran workers drift to non-natal groups? Generalized reciprocity and the maximization of group and parental success

Eusocial Hymenoptera are often characterized by having facultatively or obligately sterile worker castes. However, findings across an increasing number of species are that some workers are non-natal—they have ‘drifted’ away from where they were born and raised. Moreover, drifters are often indistinguishable from natal workers in the work and benefits provided to joined groups. This seems an evolutionary paradox of providing benefits to potentially unrelated individuals over close kin. Rather than being mistakes, drifting is proposed to be adaptive if joiners either gain inclusive fitness by preferentially moving to other kin groups or through generalized reciprocity in which exchanging workers across groups raises group-level genetic diversity and creates social heterosis. It is unclear, however, if reciprocity is unlikely because of a susceptibility to cheating. In resolving this question, a series of evolutionary simulations show: (1) Reciprocity can persist under a range of genetic assumptions and scenarios of cheating, (2) cheating almost always evolves, but can be expressed in a variety of ways that are not always predictable, (3) the inclusive fitness hypothesis is equally or more susceptible to cheating. Moreover, existing data in Hymenoptera (although not extensive) are more consistent with generalized reciprocity. This supports a hypothesis that drifting, as a phenomenon, may more often reflect maximization of group and parental fitness rather than fitness gains for the individual drifters.     

Social familiarity relaxes the constraints of limited attention and enhances reproduction of group‐living predatory mites

In many group‐living animals, within‐group associations are determined by familiarity, i.e. familiar individuals, independent of genetic relatedness, preferentially associate with each other. The ultimate causes of this behaviour are poorly understood and rigorous documentation of its adaptive significance is scarce. Limited attention theory states that focusing on a given task has interrelated cognitive, behavioural and physiological costs with respect to the attention paid to other tasks. In multiple signal environments attention has thus to be shared among signals. Assuming that familiar neighbours require less attention than unfamiliar ones, associating with familiar individuals should increase the efficiency in other tasks and ultimately increase fitness. We tested this prediction in adult females of the group‐living, plant‐inhabiting predatory mite Phytoseiulus persimilis. We evaluated the influence of social familiarity on within‐group association behaviour, activity, predation and reproduction. In mixed groups (familiar and unfamiliar), familiar predator females preferentially associated with each other. In pure groups (either familiar or unfamiliar), familiar predator females produced more eggs than unfamiliar females at similar predation rates. Higher egg production was correlated with lower activity levels, indicating decreased restlessness. In light of limited attention theory, we argue that the ability to discriminate between familiar and unfamiliar individuals and preferential association with familiar individuals confers a selective advantage because familiar social environments are cognitively and physiologically less taxing than unfamiliar social environments.     

High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp Polistes canadensis

Explaining the evolution of helping behaviour in the eusocial insects where nonreproductive (“worker”) individuals help raise the offspring of other individuals (“queens”) remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on nontropical species, where seasonality causes family groups to disperse; cofoundresses forming new nests the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here, we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes—Polistes canadensis. Using both microsatellites and newly developed single nucleotide polymorphism markers, we show that adult cofoundresses are highly related and that brood production is monopolized by a single female across the nesting cycle. Nonreproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life history and ecologies when considering the evolution of reproductive strategies.     

Genetic relatedness and group size in an aggregation economy

Summary We use Hamilton's Rule to investigate effects of genetic relatedness on the predicted size of social groups. We assume an aggregation economy; individual fitness initially increases with group size, but in sufficiently large groups each member's individual fitness declines with further increments in the size of the group. We model two processes of group formation, designated free entry and group-controlled entry. The first model assumes that solitary individuals decide to join groups or remain alone; group size equilibrates when solitaries no longer choose to join. The second model allows group members to regulate the size of the group, so that the predicted group size results from members' decisions to repel or accept intruding solitaries. Both the Nash equilibrium group size and any change in the equilibrium caused by varying the level of relatedness depend on the particular entry rule assumed. The largest equilibrium group size occurs when solitaries choose between joining or not joining and individuals are unrelated. Increasing genetic relatedness may reduce and can never increase, equilibrium group size when this entry rule applies. The smallest equilibrium group size occurs when group members choose between repelling or accepting intruders and individuals are unrelated. Under this entry rule, increasing genetic relatedness can increase and can never decrease, equilibrium group size. We extend the models' predictions to suggest when individuals should prefer kin vs non-kin as members of the same group.     

The economics of altruistic punishment and the maintenance of cooperation

Explaining the evolution and maintenance of cooperation among unrelated individuals is one of the fundamental problems in biology and the social sciences. Recent findings suggest that altruistic punishment is an important mechanism maintaining cooperation among humans. We experimentally explore the boundaries of altruistic punishment to maintain cooperation by varying both the cost and the impact of punishment, using an exceptionally extensive subject pool. Our results show that cooperation is only maintained if conditions for altruistic punishment are relatively favourable: low cost for the punisher and high impact on the punished. Our results indicate that punishment is strongly governed by its cost-to-impact ratio and that its effect on cooperation can be pinned down to one single variable: the threshold level of free-riding that goes unpunished. Additionally, actual pay-offs are the lowest when altruistic punishment maintains cooperation, because the pay-off destroyed through punishment exceeds the gains from increased cooperation. Our results are consistent with the interpretation that punishment decisions come from an amalgam of emotional response and cognitive cost-impact analysis and suggest that altruistic punishment alone can hardly maintain cooperation under multi-level natural selection. Uncovering the workings of altruistic punishment as has been done here is important because it helps predicting under which conditions altruistic punishment is expected to maintain cooperation.