Exploitative leaders incite intergroup warfare in a social mammal.

Collective conflicts among humans are widespread, although often highly destructive. A classic explanation for the prevalence of such warfare in some human societies is leadership by self-serving individuals that reap the benefits of conflict while other members of society pay the costs. Here, we show that leadership of this kind can also explain the evolution of collective violence in certain animal societies. We first extend the classic hawk-dove model of the evolution of animal aggression to consider cases in which a subset of individuals within each group may initiate fights in which all group members become involved. We show that leadership of this kind, when combined with inequalities in the payoffs of fighting, can lead to the evolution of severe intergroup aggression, with negative consequences for population mean fitness. We test our model using long-term data from wild banded mongooses, a species characterized by frequent intergroup conflicts that have very different fitness consequences for male and female group members. The data show that aggressive encounters between groups are initiated by females, who gain fitness benefits from mating with extragroup males in the midst of battle, whereas the costs of fighting are borne chiefly by males. In line with the model predictions, the result is unusually severe levels of intergroup violence. Our findings suggest that the decoupling of leaders from the costs that they incite amplifies the destructive nature of intergroup conflict.

Kinship dynamics: patterns and consequences of changes in local relatedness.

Mounting evidence suggests that patterns of local relatedness can change over time in predictable ways, a process termed kinship dynamics. Kinship dynamics may occur at the level of the population or social group, where the mean relatedness across all members of the population or group changes over time, or at the level of the individual, where an individual's relatedness to its local group changes with age. Kinship dynamics are likely to have fundamental consequences for the evolution of social behaviour and life history because they alter the inclusive fitness payoffs to actions taken at different points in time. For instance, growing evidence suggests that individual kinship dynamics have shaped the evolution of menopause and age-specific patterns of helping and harming. To date, however, the consequences of kinship dynamics for social evolution have not been widely explored. Here we review the patterns of kinship dynamics that can occur in natural populations and highlight how taking a kinship dynamics approach has yielded new insights into behaviour and life-history evolution. We discuss areas where analysing kinship dynamics could provide new insight into social evolution, and we outline some of the challenges in predicting and quantifying kinship dynamics in natural populations.

Explaining negative kin discrimination in a cooperative mammal society.

Kin selection theory predicts that, where kin discrimination is possible, animals should typically act more favorably toward closer genetic relatives and direct aggression toward less closely related individuals. Contrary to this prediction, we present data from an 18-y study of wild banded mongooses, Mungos mungo, showing that females that are more closely related to dominant individuals are specifically targeted for forcible eviction from the group, often suffering severe injury, and sometimes death, as a result. This pattern cannot be explained by inbreeding avoidance or as a response to more intense local competition among kin. Instead, we use game theory to show that such negative kin discrimination can be explained by selection for unrelated targets to invest more effort in resisting eviction. Consistent with our model, negative kin discrimination is restricted to eviction attempts of older females capable of resistance; dominants exhibit no kin discrimination when attempting to evict younger females, nor do they discriminate between more closely or less closely related young when carrying out infanticidal attacks on vulnerable infants who cannot defend themselves. We suggest that in contexts where recipients of selfish acts are capable of resistance, the usual prediction of positive kin discrimination can be reversed. Kin selection theory, as an explanation for social behavior, can benefit from much greater exploration of sequential social interactions.

Multiple Evolutionary Routes to Monogamy: Modeling the Coevolution of Mating Decisions and Parental Investment.

The relationships between mating decisions and parental investment are central to evolution, but to date few theoretical treatments of their coevolution have been developed. Here we adopt a demographically explicit, adaptive dynamics approach to analyze the coevolution of female mating decisions and parental investment of both sexes in a self-consistent way. Our models predict that where females cannot interfere with one another's mating decisions and where they do not differ in their survival and fecundity prospects, monogamy should be rare, favored only under harsh environmental conditions, in sparse populations. However, allowing for interference or asymmetries among females leads to selection for monogamy over a much broader range of environments and demographies. Interference by paired, resident females may prevent unmated rivals from joining existing monogamous pairs, thus barring the formation of polygynous groups. Asymmetries between established, primary females and subsequently joining secondary females may increase the relative costs of early polygynous reproduction, compared to delayed monogamy for the latter. The models thus highlight different routes by which monogamy may evolve. We further track how parental investment by the sexes coevolves with female mating decisions, highlighting how sexual conflict over parental investment is both cause and effect of mating behavior.

Evolutionary public health: introducing the concept.

The emerging discipline of evolutionary medicine is breaking new ground in understanding why people become ill. However, the value of evolutionary analyses of human physiology and behaviour is only beginning to be recognised in the field of public health. Core principles come from life history theory, which analyses the allocation of finite amounts of energy between four competing functions-maintenance, growth, reproduction, and defence. A central tenet of evolutionary theory is that organisms are selected to allocate energy and time to maximise reproductive success, rather than health or longevity. Ecological interactions that influence mortality risk, nutrient availability, and pathogen burden shape energy allocation strategies throughout the life course, thereby affecting diverse health outcomes. Public health interventions could improve their own effectiveness by incorporating an evolutionary perspective. In particular, evolutionary approaches offer new opportunities to address the complex challenges of global health, in which populations are differentially exposed to the metabolic consequences of poverty, high fertility, infectious diseases, and rapid changes in nutrition and lifestyle. The effect of specific interventions is predicted to depend on broader factors shaping life expectancy. Among the important tools in this approach are mathematical models, which can explore probable benefits and limitations of interventions in silico, before their implementation in human populations.

Reciprocal mimicry: kin selection can drive defended prey to resemble their Batesian mimics.

Established mimicry theory predicts that Batesian mimics are selected to resemble their defended models, while models are selected to become dissimilar from their mimics. However, this theory has mainly considered individual selection acting on solitary organisms such as adult butterflies. Although Batesian mimicry of social insects is common, the few existing applications of kin selection theory to mimicry have emphasized relatedness among mimics rather than among models. Here, we present a signal detection model of Batesian mimicry in which the population of defended model prey is kin structured. Our analysis shows for most of parameter space that increased average dissimilarity from mimics has a twofold group-level cost for the model prey: it attracts more predators and these adopt more aggressive attack strategies. When mimetic resemblance and local relatedness are sufficiently high, such costs acting in the local neighbourhood may outweigh the individual benefits of dissimilarity, causing kin selection to drive the models to resemble their mimics. This requires model prey to be more common than mimics and/or well-defended, the conditions under which Batesian mimicry is thought most successful. Local relatedness makes defended prey easier targets for Batesian mimicry and is likely to stabilize the mimetic relationship over time.

How Sex-Biased Dispersal Affects Sexual Conflict over Care.

Existing models of parental investment have mainly focused on interactions at the level of the family and have paid much less attention to the impact of population-level processes. Here we extend classical models of parental care to assess the impact of population structure and limited dispersal. We find that sex differences in dispersal substantially affect the amount of care provided by each parent, with the more philopatric sex providing the majority of care to young. This effect is most pronounced in highly viscous populations: in such cases, when classical models would predict stable biparental care, inclusion of a modest sex difference in dispersal leads to uniparental care by the philopatric sex. In addition, mating skew also affects sex differences in parental investment, with the more numerous sex providing most of the care. However, the effect of mating skew holds only when parents care for their own offspring. When individuals breed communally, we recover the previous finding that the more philopatric sex provides most of the care even when it is the rarer sex. We conclude that sex-biased dispersal is likely to be an important yet currently overlooked driver of sex differences in parental care.

Policing of reproduction by hidden threats in a cooperative mammal.

The evolution of cooperation in animal and human societies is associated with mechanisms to suppress individual selfishness. In insect societies, queens and workers enforce cooperation by "policing" selfish reproduction by workers. Insect policing typically takes the form of damage limitation after individuals have carried out selfish acts (such as laying eggs). In contrast, human policing is based on the use of threats that deter individuals from acting selfishly in the first place, minimizing the need for damage limitation. Policing by threat could in principle be used to enforce reproductive suppression in animal societies, but testing this idea requires an experimental approach to simulate reproductive transgression and provoke out-of-equilibrium behavior. We carried out an experiment of this kind on a wild population of cooperatively breeding banded mongooses (Mungos mungo) in Uganda. In this species, each group contains multiple female breeders that give birth to a communal litter, usually on the same day. In a 7-y experiment we used contraceptive injections to manipulate the distribution of maternity within groups, triggering hidden threats of infanticide. Our data suggest that older, socially dominant females use the threat of infanticide to deter selfish reproduction by younger females, but that females can escape the threat of infanticide by synchronizing birth to the same day as older females. Our study shows that reproduction in animal societies can be profoundly influenced by threats that remain hidden until they are triggered experimentally. Coercion may thus extend well beyond the systems in which acts of infanticide are common.

Who directs group movement? Leader effort versus follower preference in stickleback fish of different personality.

During collective movement, bolder individuals often emerge as leaders. Here, we investigate whether this reflects a greater propensity of bold individuals to initiate movement, or a preference for shy individuals to follow a bolder leader. We set up trios of stickleback fish comprising a focal individual who was either bold or shy, and one other individual of each personality. We then recorded the movements of all individuals in and out of cover in a foraging context to determine how assiduously the focal fish followed the movements of each other partner. We found that a shy focal fish preferred to follow a leader whose personality matched its own, but we did not detect such a difference in bold fish. Despite this preference, however, the greater propensity of bold individuals to initiate movements out of cover meant that they successfully led more joint trips. Thus, when offered a choice of leaders, sticklebacks prefer to follow individuals whose personality matches their own, but bolder individuals may, nevertheless, be able to impose their leadership, even among shy followers, simply through greater effort.

The evolution of multivariate maternal effects.

There is a growing interest in predicting the social and ecological contexts that favor the evolution of maternal effects. Most predictions focus, however, on maternal effects that affect only a single character, whereas the evolution of maternal effects is poorly understood in the presence of suites of interacting traits. To overcome this, we simulate the evolution of multivariate maternal effects (captured by the matrix M) in a fluctuating environment. We find that the rate of environmental fluctuations has a substantial effect on the properties of M: in slowly changing environments, offspring are selected to have a multivariate phenotype roughly similar to the maternal phenotype, so that M is characterized by positive dominant eigenvalues; by contrast, rapidly changing environments favor Ms with dominant eigenvalues that are negative, as offspring favor a phenotype which substantially differs from the maternal phenotype. Moreover, when fluctuating selection on one maternal character is temporally delayed relative to selection on other traits, we find a striking pattern of cross-trait maternal effects in which maternal characters influence not only the same character in offspring, but also other offspring characters. Additionally, when selection on one character contains more stochastic noise relative to selection on other traits, large cross-trait maternal effects evolve from those maternal traits that experience the smallest amounts of noise. The presence of these cross-trait maternal effects shows that individual maternal effects cannot be studied in isolation, and that their study in a multivariate context may provide important insights about the nature of past selection. Our results call for more studies that measure multivariate maternal effects in wild populations.

Kin competition and the evolution of sex differences in development time and body size.

One key trade-off underlying life-history evolution is the one between age and size at maturity, with earlier maturation leading to greater chances of juvenile survival at the cost of reduced fecundity as an adult. Here we model the impact of limited dispersal and kin competition on the stable resolution of this trade-off. We show that if mating is at least occasionally nonlocal, then limited dispersal favors juvenile survival over adult fecundity in females, promoting earlier female maturation at the population level; at the same time, it favors adult fecundity over juvenile survival in males, promoting later male maturation. Limited dispersal and local competition can thus drive the evolution of sexual dimorphism in the timing of maturation and consequent dimorphism in body size. At the individual level, if maturation can be flexibly adjusted in response to dispersal status, then both males and females who disperse as offspring should mature earlier than those who remain on their natal patch.

Evolution of positive and negative density-dependent dispersal.

Understanding the evolution of density-dependent dispersal strategies has been a major challenge for evolutionary ecologists. Some existing models suggest that selection should favour positive and others negative density-dependence in dispersal. Here, we develop a general model that shows how and why selection may shift from positive to negative density-dependence in response to key ecological factors, in particular the temporal stability of the environment. We find that in temporally stable environments, particularly with low dispersal costs and large group sizes, habitat heterogeneity selects for negative density-dependent dispersal, whereas in temporally variable environments, particularly with high dispersal costs and small group sizes, habitat heterogeneity selects for positive density-dependent dispersal. This shift reflects the changing balance between the greater competition for breeding opportunities in more productive patches, versus the greater long-term value of offspring that establish themselves there, the latter being very sensitive to the temporal stability of the environment. In general, dispersal of individuals out of low-density patches is much more sensitive to habitat heterogeneity than is dispersal out of high-density patches.

Evolution of personality differences in leadership.

When members of a group differ in their preferred course of action, coordination poses a challenge. Leadership offers one way to resolve this difficulty, but the evolution of leaders and followers is itself poorly understood. Existing discussions have frequently attributed leadership to differences in information or need among individuals. Here, however, we show that in an n-player, repeated coordination game, selection leads to evolutionary branching and diversification in intrinsic leadership among the members of a population even in the absence of any variation in state. When individuals interact in pairs, repeated branching is possible; when individuals interact in larger groups, the typical outcome is a single branching event leading to a dimorphism featuring extreme intrinsic leaders and followers. These personality types emerge and are maintained by frequency-dependent selection, because leaders gain by imposing their preferences on followers, but fail to coordinate effectively when interacting with other leaders. The fraction of intrinsic leaders in the population increases with the degree of conflict among group members, with both types common only at intermediate levels of conflict; when conflict is weak, most individuals are intrinsic followers, and groups achieve high levels of coordination by randomly converging on one individual's preferred option, whereas when conflict is strong, most individuals are intrinsic leaders, and coordination breaks down because members of a group are rarely willing to follow another.

Power and temptation cause shifts between exploitation and cooperation in a cleaner wrasse mutualism.

In many instances of cooperation, only one individual has both the potential and the incentive to 'cheat' and exploit its partner. Under these asymmetric conditions, a simple model predicts that variation in the temptation to cheat and in the potential victim's capacity for partner control leads to shifts between exploitation and cooperation. Here, we show that the threat of early termination of an interaction was sufficient to induce cleaner wrasse Labroides dimidiatus to feed selectively against their preference (which corresponds to cooperatively eating client fish ectoparasites), provided that their preference for alternative food was weak. Under opposite conditions, cleaners fed selectively according to their own preference (which corresponds to cheating by eating client mucus). By contrast, a non-cleaning fish species, Halichoeres melanurus, failed to adjust its foraging behaviour under these same conditions. Thus, cleaners appear to have evolved the power to strategically adjust their levels of cooperation according to the circumstances.

Experience overrides personality differences in the tendency to follow but not in the tendency to lead.

In many animal groups, coordinated activity is facilitated by the emergence of leaders and followers. Although the identity of leaders is to some extent predictable, most groups experience frequent changes of leadership. How do group members cope with such changes in their social role? Here, we compared the foraging behaviour of pairs of stickleback fish after a period of either (i) role reinforcement, which involved rewarding the shyer follower for following, and the bolder leader for leading, or (ii) role reversal, which involved rewarding the shyer follower for leading, and the bolder leader for following. We found that, irrespective of an individual's temperament, its tendency to follow is malleable, whereas the tendency to initiate collective movement is much more resistant to change. As a consequence of this lack of flexibility in initiative, greater temperamental differences within a pair led to improved performance when typical roles were reinforced, but to impaired performance when typical roles were reversed.

Costly lifetime maternal investment in killer whales.

Parents often sacrifice their own future reproductive success to boost the survival of their offspring, a phenomenon referred to as parental investment. In several social mammals, mothers continue to improve the survival of their offspring well into adulthood;1,2,3,4,5 however, whether this extended care comes at a reproductive costs to mothers, and therefore represents maternal investment, is not well understood. We tested whether lifetime maternal care is a form of parental investment in fish-eating "resident" killer whales. Adult killer whales, particularly males, are known to receive survival benefits from their mothers;3 however, whether this comes at a cost to mothers' reproductive success is not known. Using multiple decades of complete census data from the "southern resident" population, we found a strong negative correlation between females' number of surviving weaned sons and their annual probability of producing a viable calf. This negative effect did not attenuate as sons grew older, and the cost of sons could not be explained by long-term costs of lactation or group composition effects, supporting the hypothesis that caring for adult sons is reproductively costly. This is the first direct evidence of lifetime maternal investment in an iteroparous animal, revealing a previously unknown life history strategy.

Parents and offspring in an evolutionary game: the effect of supply on demand when costs of care vary.

Current models of parent-offspring communication do not explicitly predict the effect of parental food supply on offspring demand (ESD). However, existing theory is frequently interpreted as predicting a negative ESD, such that offspring beg less when parental supply is high. While empirical evidence largely supports this interpretation, several studies have identified the opposite case, with well-fed offspring begging more than those in poorer condition. Here, we show that signalling theory can give rise to either a negative or a positive ESD depending on the precise form of costs and benefits. Introducing variation among parents in the cost of care, we show that the ESD may change sign depending upon the quantitative relation between two effects: (i) decreased supply leads to increased begging because of an increase in marginal fitness benefit of additional resources to offspring, (ii) decreased supply leads to reduced begging because it is associated with a decrease in parental responsiveness, rendering begging less effective. To illustrate the interplay between these two effects, we show that Godfray's seminal model of begging yields a negative ESD when care is generally cheap, because the impact of supply on the marginal benefits of additional resources then outweighs the associated changes in parental responsiveness to begging. By contrast, the same model predicts a positive ESD when care is generally costly, because the impact of care costs on parental responsiveness then outweighs the change in marginal benefits.

Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects.

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister-sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that 'family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism'.

Untangling the oxidative cost of reproduction: An analysis in wild banded mongooses.

The cost of reproduction plays a central role in evolutionary theory, but the identity of the underlying mechanisms remains a puzzle. Oxidative stress has been hypothesized to be a proximate mechanism that may explain the cost of reproduction. We examine three pathways by which oxidative stress could shape reproduction. The "oxidative cost" hypothesis proposes that reproductive effort generates oxidative stress, while the "oxidative constraint" and "oxidative shielding" hypotheses suggest that mothers mitigate such costs through reducing reproductive effort or by pre-emptively decreasing damage levels, respectively. We tested these three mechanisms using data from a long-term food provisioning experiment on wild female banded mongooses (Mungos mungo). Our results show that maternal supplementation did not influence oxidative stress levels, or the production and survival of offspring. However, we found that two of the oxidative mechanisms co-occur during reproduction. There was evidence of an oxidative challenge associated with reproduction that mothers attempted to mitigate by reducing damage levels during breeding. This mitigation is likely to be of crucial importance, as long-term offspring survival was negatively impacted by maternal oxidative stress. This study demonstrates the value of longitudinal studies of wild animals in order to highlight the interconnected oxidative mechanisms that shape the cost of reproduction.

Patterns and consequences of age-linked change in local relatedness in animal societies.

The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness-the average relatedness of an individual to their social environment-therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual's lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.