Michael A. Cant

Reproductive skew and the threat of eviction: a new perspective

Most recent models of the partitioning of reproduction attempt to explain patterns of skew on the assumption that dominant individuals have complete control over breeding opportunities within the group, but may nevertheless concede a share of direct reproduction to subordinates as an incentive to remain peacefully in the association. Although these models may be applicable to some animal societies, we argue that they fail to provide a comprehensive theory of skew. Instead, we suggest that subordinates may often be able to claim unsanctioned reproduction for themselves, but will be forced to exercise a degree of reproductive restraint lest they incite ejection by the dominant. Reproductive skew, in other words, may reflect the threat of ejection (inducing subordinate restraint) rather than the threat of subordinate departure (inducing reproductive concessions by dominants). We present a simple ESS model of reproductive skew under these circumstances, which demonstrates that a shift in emphasis from reproductive concessions by dominants to reproductive restraint on the part of subordinates, radically alters the predictions of skew models. High group productivity, high relatedness and (when group members are related) strong ecological constraints are all expected to lead to reduced skew (the opposite conclusions to those of previous, concession-based analyses). The reason is that these factors reduce the benefits (or increase the costs) of ejection to the dominant, who therefore does best to tolerate more subordinate reproduction.

Social control of reproduction in banded mongooses

Recent theoretical work suggests that the distribution of reproduction, or degree of reproductive skew, in animal societies depends crucially on (1) whether dominant individuals can fully control subordinate reproduction, and (2) how subordinate reproduction affects the fitness of dominants. I investigated these two factors in cooperatively breeding banded mongooses, Mungos mungo. Female packmates entered oestrus together and were closely guarded by dominant males. These males were aggressive to subordinate males who attempted to mate, but females still managed to mate with males other than their mate guard. Older females were guarded and mated a few days before their younger packmates, yet all females usually gave birth on the same day, suggesting that older females may have a longer gestation period. Moreover, older females carried more fetuses. Overall, ca. 83% of adult females conceived in each breeding attempt and 71% carried to term. These results indicate that, among males, dominant individuals did not have full control over the mating attempts of subordinates (since they could not fully control the mating behaviour of the females they guarded), while among females there was little or no attempt to prevent subordinates from breeding (at least, prior to parturition). Two within-group infanticides by males suggested that some control over reproduction may be exercised postpartum. Per capita survivorship of young in the den increased with the number of females who gave birth. Thus, dominant females may benefit from subordinate reproduction, providing a possible explanation for the lack of reproductive suppression among females in this species. Copyright 2000 The Association for the Study of Animal Behaviour.

Helping effort and future fitness in cooperative animal societies

Little attention has been paid to a conspicuous and universal feature of animal societies: the variation between individuals in helping effort. Here, we develop a multiplayer kin–selection model that assumes that subordinates face a trade–off because current investment in help reduces their own future reproductive success. The model makes two predictions: (i) subordinates will work less hard the closer they are to inheriting breeding status; and (ii) for a given dominance rank, subordinates will work less hard in larger groups. The second prediction reflects the larger pay–off from inheriting a larger group. Both predictions were tested through a field experiment on the paper wasp Polistes dominulus. First, we measured an index of helping effort among subordinates, then we removed successive dominants to reveal the inheritance ranks of the subordinates: their positions in the queue to inherit dominance. We found that both inheritance rank and group size had significant effects on helping effort, in the manner predicted by our model. The close match between our theoretical and empirical results suggests that individuals adjust their helping effort according to their expected future reproductive success. This relationship has probably remained hidden in previous studies that have focused on variation in genetic relatedness.

Reproductive conflict and the separation of reproductive generations in humans

An enduring puzzle of human life history is why women cease reproduction midway through life. Selection can favor postreproductive survival because older females can help their offspring to reproduce. But the kin-selected fitness gains of helping appear insufficient to outweigh the potential benefits of continued reproduction. Why then do women cease reproduction in the first place? Here, we suggest that early reproductive cessation in humans is the outcome of reproductive competition between generations, and we present a simple candidate model of how this competition will be resolved. We show that among primates exhibiting a postreproductive life span, humans exhibit an extraordinarily low degree of reproductive overlap between generations. The rapid senescence of the human female reproductive system coincides with the age at which, in natural fertility populations, women are expected to encounter reproductive competition from breeding females of the next generation. Several lines of evidence suggest that in ancestral hominids, this younger generation typically comprised immigrant females. In these circumstances, relatedness asymmetries within families are predicted to give younger females a decisive advantage in reproductive conflict with older females. A model incorporating both the costs of reproductive competition and the benefits of grandmothering can account for the timing of reproductive cessation in humans and so offers an improved understanding of the evolution of menopause.

A model for the evolution of reproductive skew without reproductive suppression

Reproductive skew is a measure of the way breeding is distributed among the members of an animal society or group. Up to now, explanations of patterns of skew have been limited to one particular model, which assumes that a single dominant has full control over the distribution of subordinate reproduction. If this control is incomplete or absent, however, unsanctioned breeding by subordinate females will increase the total number of young produced. Here I present a new model for the evolution of skew that considers the effect of brood size on the inclusive fitness of dominants and subordinates. By augmenting brood size, a subordinate female reduces the per capita fitness of a dominants offspring, so the net benefits of producing young are lower for related subordinates. I consider the stable level of skew when both dominant and subordinate attempt to maximize their inclusive fitness under two conditions: (1) when the dominant is unable to anticipate that a subordinate will add to her brood; and (2) the dominant does anticipate subordinate reproduction and can respond by adjusting her own brood size. In the first case, the model predicts that reproductive skew will increase with relatedness between breeders, because related subordinates are selected to add fewer young to the dominants brood. In the second case, the dominants optimal response to the presence of a second breeder exaggerates the relationship between relatedness and skew: dominants should produce more young when breeding with related compared with unrelated subordinates. Copyright 1998 The Association for the Study of Animal Behaviour.

The evolution of menopause in cetaceans and humans: the role of demography

Human females stop reproducing long before they die. Among other mammals, only pilot and killer whales exhibit a comparable period of post-reproductive life. The grandmother hypothesis suggests that kin selection can favour post-reproductive survival when older females help their relatives to reproduce. But although there is an evidence that grandmothers can provide such assistance, it is puzzling why menopause should have evolved only among the great apes and toothed whales. We have previously suggested (Cant & Johnstone 2008 Proc. Natl Acad. Sci. USA 105, 5332–5336 (doi:10.1073/pnas.0711911105)) that relatedness asymmetries owing to female-biased dispersal in ancestral humans would have favoured younger females in reproductive competition with older females, predisposing our species to the evolution of menopause. But this argument appears inapplicable to menopausal cetaceans, which exhibit philopatry of both sexes combined with extra-group mating. Here, we derive general formulae for ‘kinship dynamics’, the age-related changes in local relatedness that occur in long-lived social organisms as a consequence of dispersal and mortality. We show that the very different social structures of great apes and menopausal whales both give rise to an increase in local relatedness with female age, favouring late-life helping. Our analysis can therefore help to explain why, of all long-lived, social mammals, it is specifically among the great apes and toothed whales that menopause and post-reproductive helping have evolved.

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.

Eviction and dispersal in co-operatively breeding banded mongooses (Mungos mungo)

The mode by which individuals disperse, and the cost of dispersal, are of great importance in attempts to understand variation in reproductive skew in animal societies. In this paper we report detailed information on dispersal and pack formation in banded mongooses Mungos mungo. Six pack fission events were recorded among 11 packs over 22 months. Pack fission occurred under two distinct circumstances. First, groups of individuals were evicted from their natal group as a result of intense aggression from other group members. A small fraction of group members was responsible for most of the aggression. Both sexes helped to attack and evict individuals from the group, and both males and females were driven out of their natal groups en masse. The second mode of pack fission occurred when groups of same-sex individuals left their natal group voluntarily to join dispersing individuals of the opposite sex, thereby forming new packs. Dispersing groups were more frequently involved in fights with rival packs of mongooses compared to established groups, and in one instance these fights seemed to be responsible for severe injury and increased mortality among members of a dispersing group. The observations of eviction provide one line of evidence that the presence of subordinates is sometimes detrimental to dominants, contrary to the assumptions of concession models of reproductive skew.

Individual Variation in Social Aggression and the Probability of Inheritance: Theory and a Field Test

Recent theory suggests that much of the wide variation in individual behavior that exists within cooperative animal societies can be explained by variation in the future direct component of fitness, or the probability of inheritance. Here we develop two models to explore the effect of variation in future fitness on social aggression. The models predict that rates of aggression will be highest toward the front of the queue to inherit and will be higher in larger, more productive groups. A third prediction is that, in seasonal animals, aggression will increase as the time available to inherit the breeding position runs out. We tested these predictions using a model social species, the paper wasp Polistes dominulus. We found that rates of both aggressive “displays” (aimed at individuals of lower rank) and aggressive “tests” (aimed at individuals of higher rank) decreased down the hierarchy, as predicted by our models. The only other significant factor affecting aggression rates was date, with more aggression observed later in the season, also as predicted. Variation in future fitness due to inheritance rank is the hidden factor accounting for much of the variation in aggressiveness among apparently equivalent individuals in this species.

Reproductive control via eviction (but not the threat of eviction) in banded mongooses.

Considerable research has focused on understanding variation in reproductive skew in cooperative animal societies, but the pace of theoretical development has far outstripped empirical testing of the models. One major class of model suggests that dominant individuals can use the threat of eviction to deter subordinate reproduction (the ‘restraint’ model), but this idea remains untested. Here, we use long-term behavioural and genetic data to test the assumptions of the restraint model in banded mongooses (Mungos mungo), a species in which subordinates breed regularly and evictions are common. We found that dominant females suffer reproductive costs when subordinates breed, and respond to these costs by evicting breeding subordinates from the group en masse, in agreement with the assumptions of the model. We found no evidence, however, that subordinate females exercise reproductive restraint to avoid being evicted in the first place. This means that the pattern of reproduction is not the result of a reproductive ‘transaction’ to avert the threat of eviction. We present a simple game theoretical analysis that suggests that eviction threats may often be ineffective to induce pre-emptive restraint among multiple subordinates and predicts that threats of eviction (or departure) will be much more effective in dyadic relationships and linear hierarchies. Transactional models may be more applicable to these systems. Greater focus on testing the assumptions rather than predictions of skew models can lead to a better understanding of how animals control each others reproduction, and the extent to which behaviour is shaped by overt acts versus hidden threats.