Leaders of war: modelling the evolution of conflict among heterogeneous groups.

War, in human and animal societies, can be extremely costly but can also offer significant benefits to the victorious group. We might expect groups to go into battle when the potential benefits of victory (V) outweigh the costs of escalated conflict (C); however, V and C are unlikely to be distributed evenly in heterogeneous groups. For example, some leaders who make the decision to go to war may monopolize the benefits at little cost to themselves ('exploitative' leaders). By contrast, other leaders may willingly pay increased costs, above and beyond their share of V ('heroic' leaders). We investigated conflict initiation and conflict participation in an ecological model where single-leader-multiple-follower groups came into conflict over natural resources. We found that small group size, low migration rate and frequent interaction between groups increased intergroup competition and the evolution of 'exploitative' leadership, while converse patterns favoured increased intragroup competition and the emergence of 'heroic' leaders. We also found evidence of an alternative leader/follower 'shared effort' outcome. Parameters that favoured high contributing 'heroic' leaders, and low contributing followers, facilitated transitions to more peaceful outcomes. We outline and discuss the key testable predictions of our model for empiricists studying intergroup conflict in humans and animals. This article is part of the theme issue 'Intergroup conflict across taxa'.

A veil of ignorance can promote fairness in a mammal society.

Rawls argued that fairness in human societies can be achieved if decisions about the distribution of societal rewards are made from behind a veil of ignorance, which obscures the personal gains that result. Whether ignorance promotes fairness in animal societies, that is, the distribution of resources to reduce inequality, is unknown. Here we show experimentally that cooperatively breeding banded mongooses, acting from behind a veil of ignorance over kinship, allocate postnatal care in a way that reduces inequality among offspring, in the manner predicted by a Rawlsian model of cooperation. In this society synchronized reproduction leaves adults in a group ignorant of the individual parentage of their communal young. We provisioned half of the mothers in each mongoose group during pregnancy, leaving the other half as matched controls, thus increasing inequality among mothers and increasing the amount of variation in offspring birth weight in communal litters. After birth, fed mothers provided extra care to the offspring of unfed mothers, not their own young, which levelled up initial size inequalities among the offspring and equalized their survival to adulthood. Our findings suggest that a classic idea of moral philosophy also applies to the evolution of cooperation in biological systems.

Parental effects and the evolution of phenotypic memory.

Despite growing evidence for nongenetic inheritance, the ecological conditions that favour the evolution of heritable parental or grandparental effects remain poorly understood. Here, we systematically explore the evolution of parental effects in a patch-structured population with locally changing environments. When selection favours the production of a mix of offspring types, this mix differs according to the parental phenotype, implying that parental effects are favoured over selection for bet-hedging in which the mixture of offspring phenotypes produced does not depend on the parental phenotype. Positive parental effects (generating a positive correlation between parental and offspring phenotype) are favoured in relatively stable habitats and when different types of local environment are roughly equally abundant, and can give rise to long-term parental inheritance of phenotypes. By contrast, unstable habitats can favour negative parental effects (generating a negative correlation between parental and offspring phenotype), and under these circumstances, even slight asymmetries in the abundance of local environmental states select for marked asymmetries in transmission fidelity.

How should parents adjust the size of their young in response to local environmental cues?

Models of parental investment typically assume that populations are well mixed and homogeneous and have devoted little attention to the impact of spatial variation in the local environment. Here, in a patch-structured model with limited dispersal, we assess to what extent resource-rich and resource-poor mothers should alter the size of their young in response to the local environment in their patch. We show that limited dispersal leads to a correlation between maternal and offspring environments, which favours plastic adjustment of offspring size in response to local survival risk. Strikingly, however, resource-poor mothers are predicted to respond more strongly to local survival risk, whereas resource-rich mothers are predicted to respond less strongly. This lack of sensitivity on the part of resource-rich mothers is favoured because they accrue much of their fitness through dispersing young. By contrast, resource-poor mothers accrue a larger fraction of their fitness through philopatric young and should therefore respond more strongly to local risk. Mothers with more resources gain a larger share of their fitness through dispersing young partly because their fitness in the local patch is constrained by the limited number of local breeding spots. In addition, when resource variation occurs at the patch level, the philopatric offspring of resource-rich mothers face stronger competition from the offspring of other local mothers, who also enjoy abundant resources. The effect of limited local breeding opportunities becomes less pronounced as patch size increases, but the impact of patch-level variation in resources holds up even with many breeders per patch.

Sexual selection and condition-dependence.

The handicap theory of sexual selection suggests that females prefer mates who display extravagant ornaments that advertise their quality or condition. It is often assumed that as such ornamental traits undergo sexually-selected exaggeration, they must inevitably become more sensitive to condition, and thus more informative. Here, we show that this is not necessarily the case. Depending on the precise form of the relationship between trait size and cost, expression may become more or less condition-dependent as the trait undergoes exaggeration, or may remain unchanged. This leads us to question how much of the information content of sexual signals can be attributed to sexual selection, and how much to pre-existing, naturally-selected condition-dependence.

Mutualism, market effects and partner control.

Intraspecific cooperation and interspecific mutualism often feature a marked asymmetry in the scope for exploitation. Cooperation may nevertheless persist despite one-sided opportunities for cheating, provided that the partner vulnerable to exploitation has sufficient control over the duration of interaction. The effectiveness of the threat of terminating an encounter, however, depends upon the ease with which both the potential victim and the potential exploiter can find replacement partners. Here, we extend a simple, game-theoretical model of this form of partner control to incorporate variation in the relative abundance of potential victims and exploiters, which leads to variation in the time required for individuals of each type to find a new partner. We show that such market effects have a dramatic influence on the stable level of exploitation (and consequent duration of interaction). As the relative abundance of victims decreases, they become less tolerant to exploitation, terminating encounters earlier (for a given level of exploitation), whereas exploiters behave in a more cooperative manner. As a result, the stable duration of interaction actually increases, despite the decreasing tolerance of the victims. Below a critical level of relative victim abundance, the model suggests that the cost of finding a replacement partner becomes so great that it does not pay to exploit at all.

Parental investment with a superior alien in the brood.

When a parent's parentage differs across breeding attempts, established theory predicts that the parent should invest more in a brood when perceived parentage is high. We present a model of parental investment in which offspring unrelated to the parent have a competitive advantage over the parent's own offspring and take a larger share of investment. We show that this can weaken or, if the competitive advantage is great, reverse the predicted relationship between perceived parentage and parental investment. A moderate competitive advantage of extra-pair young over within-pair young could partly explain the lack of any clear relationship between paternal care and paternity in many studies, and could easily arise if females choose extra-pair partners for good genes. Our results are also relevant to interspecific avian brood parasitism. As parasites reared together with host offspring are often superior competitors, their hosts could benefit from increasing investment in response to suspected parasitism.

Begging and sibling competition: how should offspring respond to their rivals?

Godfray's influential model of competitive begging predicted that offspring should respond to each other's behavior, displaying more intensely when competing with needier rivals. Empirical tests of this prediction have, however, yielded equivocal results. Here, I develop a series of evolutionarily stable strategy models of begging as a signal of need, which show that this prediction holds only for competitive aspects of display that influence the division of food among the brood. No such response is expected for cooperative begging (which influences the total level of provisioning by the parent), and the models even predict the opposite trend under some circumstances (where the indirect costs of extracting additional resources from the parent are high). These contrasting sets of predictions may help to explain the varying empirical results obtained by studies of sibling interaction. Cooperative (as opposed to competitive) begging is likely to be of greater significance in cases where dominant young can gain direct control of allocation (or enjoy some competitive advantage). Dominants are then predicted to parasitize the efforts of their weaker rivals and reduce their own investment in cooperative signaling while continuing to claim a disproportionately large share of the resources provided by the parent.

Eavesdropping and animal conflict.

Fights between pairs of animals frequently take place within a wider social context. The displays exchanged during conflict, and the outcome of an encounter, are often detectable by individuals who are not immediately involved. In at least some species, such bystanders are known to eavesdrop on contests between others, and to modify their behavior toward the contestants in response to the observed interaction. Here, I extend Maynard Smith's well known model of animal aggression, the Hawk-Dove game, to incorporate the possibility of eavesdroppers. I show that some eavesdropping is favored whenever the cost of losing an escalated fight exceeds the value of the contested resource, and that its equilibrium frequency is greatest when costs are relatively high. Eavesdropping reduces the risk of escalated conflict relative to that expected by chance, given the level of aggression in the population. However, it also promotes increased aggression, because it enhances the value of victory. The net result is that escalated conflicts are predicted to occur more frequently when eavesdropping is possible.

Cooperation in the dark: signalling and collective action in quorum-sensing bacteria.

The study of quorum-sensing bacteria has revealed a widespread mechanism of coordinating bacterial gene expression with cell density. By monitoring a constitutively produced signal molecule, individual bacteria can limit their expression of group-beneficial phenotypes to cell densities that guarantee an effective group outcome. In this paper, we attempt to move away from a commonly expressed view that these impressive feats of coordination are examples of multicellularity in prokaryotic populations. Here, we look more closely at the individual conflict underlying this cooperation, illustrating that, even under significant levels of genetic conflict, signalling and resultant cooperative behaviour can stably exist. A predictive two-trait model of signal strength and of the extent of cooperation is developed as a function of relatedness (reflecting multiplicity of infection) and basic population demographic parameters. The model predicts that the strength of quorum signalling will increase as conflict (multiplicity of infecting strains) increases, as individuals attempt to coax more cooperative contributions from their competitors, leading to a devaluation of the signal as an indicator of density. Conversely, as genetic conflict increases, the model predicts that the threshold density for cooperation will increase and the subsequent strength of group cooperation will be depressed.

The evolution of cooperative breeding through group augmentation.

Some individuals (helpers) in cooperatively breeding species provide alloparental care and often suppress their own reproduction. Kin selection is clearly an important explanation for such behaviour, but a possible alternative is group augmentation where individuals survive or reproduce better in large groups and where it therefore pays to recruit new members to the group. The evolutionary stability of group augmentation is currently disputed. We model evolutionarily stable helping strategies by following the dynamics of social groups with varying degrees of subordinate help. We also distinguish between passive augmentation, where a group member benefits from the mere presence of others, and active augmentation, where their presence as such is neutral or harmful, but where helping to recruit new group members may still be beneficial if they in turn actively provide help for the current reproductives ('delayed reciprocity'). The results show that group augmentation (either passive or active) can be evolutionarily stable and explain costly helping by non-reproductive subordinates, either alone or leading to elevated help levels when acting in concert with kin selection. Group augmentation can thus potentially explain the weak relationships between relatedness and helping behaviour that are observed in some cooperatively breeding species. In some cases, the superior mutualistic performance of cooperatively behaving groups can generate an incentive to stay and help which is strong enough to make ecological constraints unnecessary for explaining the stability of cooperatively breeding groups.

Begging and bleating: the evolution of parent-offspring signalling.

The evolution of biological signalling in the face of evolutionary conflicts of interest is an active area of evolutionary ecology, and one to which Maynard Smith has made important contributions. We explore the major theoretical challenges in the field, concentrating largely on how offspring signal to their parents when there is the potential for parent-offspring conflict. Costly offspring solicitation (begging etc.) has been interpreted in terms of a Zahavi Grafen honest handicap signal, but this has been challenged on the grounds of' the costs of signalling. We review this controversy and also explore the issue of pooling versus separating signalling equilibrium. An alternative explanation for costly begging is that it is due to sibling competition, and we discuss the relationship between these ideas and signalling models in families with more than one offspring. Finally we consider signal uncertainty, how signalling models can be made dynamic, and briefly how they may be tested experimentally.

Coalition formation in animals and the nature of winner and loser effects.

Coalition formation has been documented in a diverse array of taxa, yet there has been little formal analysis of polyadic interactions such as coalitions. Here, we develop an optimality model which examines the role of winner and loser effects in shaping coalition formation. We demonstrate that the predicted patterns of alliances are strongly dependent on the way in which winner and loser effects change with contestant strength. When winner and loser effects decrease with the resource-holding power (RHP) of the combatants, coalitions will be favoured between the strongest members of a group, but not between the weakest. If, in contrast, winner and loser effects increase with RHP, exactly the opposite predictions emerge. All other things being equal, intervention is more likely to prove worthwhile when the beneficiary of the aid is weaker (and its opponent is stronger), because the beneficiary is then less likely to win without help. Consequently, intervention is more probable when the impact of victory on the subsequent performance of a combatant increases with that individual's strength because this selects for intervention in favour of weaker combatants. The published literature on hierarchy formation does not reveal how winner and loser effects actually change with contestant strength and we therefore hope that our model will spur others to collect such data; in this light we suggest an experiment which will help to elucidate the nature of winner and loser effects and their impact on coalition formation in animals.

Signaling of need, sibling competition, and the cost of honesty.

Young birds and mammals frequently solicit food by means of extravagant and apparently costly begging displays. Much attention has been devoted to the idea that these displays are honest signals of need, and that their apparent cost serves to maintain their honesty. Recent analyses, however, have shown that the cost needed to maintain a fully informative, honest signal may often be so great that both offspring (signaler) and parent (receiver) would do better to refrain from communication. This apparently calls into question the relevance of the costly signaling hypothesis. Here, I show that this argument overlooks the impact of sibling competition. When multiple signalers must compete for the attention of a receiver (as is commonly the case in parent-offspring interactions), I show that (all other things being equal) individual equilibrium signal costs will typically be lower. The greater the number of competitors, the smaller the mean cost, though the maximum level of signal intensity employed by very needy signalers may actually increase with the number of competitors. At the same time, costs become increasingly sensitive to relatedness among signalers as opposed to relatedness between signalers and receivers. As a result of these trends, signaling proves profitable for signalers under a much wider range of conditions when there is competition (though it is still likely to be unprofitable for receivers).

Reproductive Skew in Multimember Groups.

Cooperative societies vary in the extent to which reproduction is skewed toward one or a few socially dominant animals. Many recent models attempt to explain this variation on the basis that a dominant who benefits from the presence of subordinates may offer them incentives, in the form of reproductive opportunities, to remain in the group. While most societies contain multiple members, however, these models have considered only the relationship between a dominant and a single subordinate or have assumed that all subordinates are identical. We develop an incentive-based evolutionary stable strategy model of reproductive skew in three-member groups, in which subordinates may vary in their opportunities for independent reproduction, their contribution to group productivity, and in their relatedness both to the dominant and to one another. Our model demonstrates that the conclusions of two-member models cannot all be generalized to larger groups. For example, relatedness among group members can influence whether or not the dominant does best to offer staying incentives to subordinates in a three-member, but not a two-member, group. Both the degree of skew and group stability depend on the relatedness between subordinates as well as on the relatedness of each to the dominant, and the incentives that each individual subordinate receives are influenced by the traits of the other. Whether such effects increase or decrease skew and group stability depends crucially on whether a third group member increases group productivity to a greater or lesser extent than the first.

Efficacy and honesty in communication between relatives.

The evolution of honest communication has recently become the focus of intense theoretical attention. However, strategic models dealing with honesty have largely ignored the implications of noise and perceptual error for signal evolution (just as models dealing with signal detection in the presence of noise ignore strategic issues). Here, I analyze an extended version of Maynard Smith's strategic model of signaling of need between relatives, the Philip Sidney game, that incorporates the possibility of perceptual error. I show that even in the presence of noise, there exists over a wide range of parameter values a unique, continuously stable signaling equilibrium, at which the signaler employs a costly display when needy but refrains from doing so when healthy. For a subset of this range, there also exists a second, lower cost signaling equilibrium that is not continuously stable. At the former equilibrium, predicted signal cost is inversely related to the coefficient of relatedness (r) between signaler and receiver. Cost is not, however, predicted to drop to zero even when r = 1 and there is no conflict of interest between the two (as is the case in errofree models), because it serves to enhance the efficacy of communication as well as to discourage deceit. Equilibrium signal cost is inversely related to the probability that the signaler is needy, and tends to increase with the level of noise. If noise becomes too great (i.e., if a detectable signal is too costly to produce), signaling is no longer stable; surprisingly, it is also unstable if the level of noise is too low (i.e., if a detectable signal is too cheap to produce).

Begging the question: are offspring solicitation behaviours signals of need?

Throughout the animal kingdom, distinctive behaviour by offspring commonly precedes and accompanies their provisioning by parents. Here, we assess empirical support for the recent theory that begging advertises offspring need, that parents provision young in relation to begging intensity, and that the apparently costly nature of begging ensures the reliability of the signal. While there is some support for the predictions of honest signalling models, empirical work has also revealed a host of complexities (such as the use of multiple signals) that existing theoretical analyses have only begun to address.