Reproductive skew in female common marmosets: what can proximate mechanisms tell us about ultimate causes?

Common marmosets are cooperatively breeding monkeys that exhibit high reproductive skew: most subordinate females fail to reproduce, while others attempt to breed but produce very few surviving infants. An extensive dataset on the mechanisms limiting reproduction in laboratory-housed and free living subordinate females provides unique insights into the causes of reproductive skew. Non-breeding adult females undergo suppression of ovulation and inhibition of sexual behaviour; however, they receive little or no aggression or mating interference by dominants and do not exhibit behavioural or physiological signs of stress. Breeding subordinate females receive comparable amounts of aggression to non-breeding females but are able to conceive, gestate and lactate normally. In groups containing two breeding females,however, both dominant and subordinate breeders kill one another's infants. These findings suggest that preconception reproductive suppression is not imposed on subordinate females by dominants, at a proximate level, but is instead self-imposed by most subordinates, consistent with restraint models of reproductive skew. In contrast to restraint models, however, this self-suppression probably evolved not in response to the threat of eviction by dominant females but in response to the threat of infanticide. Thus,reproductive skew in this species appears to be generated predominantly by subordinate self-restraint, in a proximate sense, but ultimately by dominant control over subordinates' reproductive attempts.     

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 other''s reproduction, and the extent to which behaviour is shaped by overt acts versus hidden threats.     

Reproductive skew, concessions and limited control

Models of reproductive skew in cooperative and eusocial societies suggest that dominants allow subordinates to breed to induce them to remain peaceably in the group. However, it is not yet clear how widely the assumptions of these models apply to animal societies, and many of the trends that they predict are consistent with the simpler suggestion that there is a struggle for reproduction between dominants and subordinates, whose outcome depends on the potential costs and benefits of the contest to both parties. Models of reproductive skew that incorporate contests of this kind and empirical studies that can discriminate clearly between reproductive concessions and failures of control are now needed.     

Patterns of reproductive skew in the polygynandrous acorn woodpecker

We compared observed levels of reproductive skew in the cooperatively breeding acorn woodpecker (Melanerpes formicivorus) with those predicted by two alternative transactional models. "Concession" models predict the degree to which parentage is shared assuming that a single dominant is in complete control of reproduction. Alternatively, "restraint" models predict reproductive sharing assuming that the dominant controls only whether subordinates remain in the group but does not control its share of reproduction. Reproductive skew is high among males: on average, the most successful male sires more than three times as many offspring as the next most successful male. Females share parentage equally and have lower constraints on dispersal and lower survival rates compared with males, which is consistent with predictions from the concessions model. Also as predicted by the concessions model, yearly variation in opportunities for dispersal before the breeding season correlates positively with skew. However, in contrast to concessions but consistent with the restraint model, skew decreases with relatedness. Thus, neither model consistently predicts patterns of reproductive skew in this species. We suggest that models of reproductive skew will need to include competitive interactions among potential breeders and mate choice before they will adequately predict patterns of reproductive partitioning in most vertebrate societies.     

The cost of dominance: suppressing subordinate reproduction affects the reproductive success of dominant female banded mongooses

Social species show considerable variation in the extent to which dominant females suppress subordinate reproduction. Much of this variation may be influenced by the cost of active suppression to dominants, who may be selected to balance the need to maximize the resources available for their own offspring against the costs of interfering with subordinate reproduction. To date, the cost of reproductive suppression has received little attention, despite its potential to influence the outcome of conflict over the distribution of reproduction in social species. Here, we investigate possible costs of reproductive suppression in banded mongooses, where dominant females evict subordinates from their groups, thereby inducing subordinate abortion. We show that evicting subordinate females is associated with substantial costs to dominant females: pups born to females who evicted subordinates while pregnant were lighter than those born after undisturbed gestations; pups whose dependent period was disrupted by an eviction attained a lower weight at independence; and the proportion of a litter that survived to independence was reduced if there was an eviction during the dependent period. To our knowledge, this is the first empirical study indicating a possible cost to dominants in attempting to suppress subordinate breeding, and we argue that much of the variation in reproductive skew both within and between social species may be influenced by adaptive variation in the effort invested in suppression by dominants.     

Sociality, mating system and reproductive skew in marmots: evidence and hypotheses

Marmot species exhibit a great diversity of social structure, mating systems and reproductive skew. In particular, among the social species (i.e. all except Marmota monax), the yellow-bellied marmot appears quite different from the others. The yellow-bellied marmot is primarily polygynous with an intermediate level of sociality and low reproductive skew among females. In contrast, all other social marmot species are mainly monogamous, highly social and with marked reproductive skew among females. To understand the evolution of this difference in reproductive skew, I examined four possible explanations identified from reproductive skew theory. From the literature, I then reviewed evidence to investigate if marmot species differ in: (1) the ability of dominants to control the reproduction of subordinates; (2) the degree of relatedness between group members; (3) the benefit for subordinates of remaining in the social group; and (4) the benefit for dominants of retaining subordinates. I found that the optimal skew hypothesis may apply for both sets of species. I suggest that yellow-bellied marmot females may benefit from retaining subordinate females and in return have to concede them reproduction. On the contrary, monogamous marmot species may gain by suppressing the reproduction of subordinate females to maximise the efficiency of social thermoregulation, even at the risk of departure of subordinate females from the family group. Finally, I discuss scenarios for the simultaneous evolution of sociality, monogamy and reproductive skew in marmots.     

Transactional skew and assured fitness return models fail to predict patterns of cooperation in wasps

Cooperative breeders often exhibit reproductive skew, where dominant individuals reproduce more than subordinates. Two approaches derived from Hamilton's inclusive fitness model predict when subordinate behavior is favored over living solitarily. The assured fitness return (AFR) model predicts that subordinates help when they are highly likely to gain immediate indirect fitness. Transactional skew models predict dominants and subordinates "agree" on a level of reproductive skew that induces subordinates to join groups. We show the AFR model to be a special case of transactional skew models that assumes no direct reproduction by subordinates. We use data from 11 populations of four wasp species (Polistes, Liostenogaster) as a test of whether transactional frameworks suffice to predict when subordinate behavior should be observed in general and the specific level of skew observed in cooperative groups. The general prediction is supported; in 10 of 11 cases, transactional models correctly predict presence or absence of cooperation. In contrast, the specific prediction is not consistent with the data. Where cooperation occurs, the model accurately predicts highly biased reproductive skew between full sisters. However, the model also predicts that distantly related or unrelated females should cooperate with low skew. This prediction fails: cooperation with high skew is the observed norm. Neither the generalized transactional model nor the special-case AFR model can explain this significant feature of wasp sociobiology. Alternative, nontransactional hypotheses such as parental manipulation and kin recognition errors are discussed.     

Social queuing in animal societies: a dynamic model of reproductive skew

Previously developed models of reproductive skew have overlooked one of the main reasons why subordinates might remain in a group despite restricted opportunities to breed: the possibility of social queuing, i.e. acquiring dominant status in the future. Here, we present a dynamic ESS model of skew in animal societies that incorporates both immediate and future fitness consequences of the decisions taken by group members, based on their probability of surviving from one season to the next (when post-breeding survival probabilities drop to zero, our analysis reduces to the model produced by Reeve and Ratnieks in 1993, which considered only a single breeding season). This allows us to compare the delayed benefits of philopatry and the immediate opportunities for independent breeding. We show that delayed benefits greatly reduce the need for dominants to offer reproductive concessions to retain subordinates peacefully in the group. Moreover, this effect is strong enough that differences in survival have a much greater impact on the group structure than differences in other parameters, such as relatedness. When the possibility of acceding to dominant status is taken into account, groups where the dominant completely monopolizes reproduction can be stable, even if they consist of unrelated individuals, and even if subordinates have a reasonably high probability of winning a fight for dominance. Finally, we show that stable groups are possible even if association leads to a decrease in current productivity. Subordinates may still stand to gain from group membership under these circumstances, as acquiring breeding positions by queuing may be more efficient than the attempt to establish a new territory. At the same time, the dominant may be unable to exclude unwelcome subordinates, may enjoy increased survival when they are present, or may gain indirect benefits from allowing relatives to stay and queue for dominance. We conclude that reproductive skew in animal groups, ranging from eusocial insect colonies to mating aggregations (leks), will be strongly influenced by the future prospects of group members.     

Predicting the temporal dynamics of reproductive skew and group membership in communal breeders

Reproductive skew models attempt to predict the fraction ofreproduction contributed by each individual that participatesin a communal brood. One potential limitation of these modelsis that individuals make a single, fixed decision about groupmembership and reproductive allocation at the beginning of thebreeding period. While this is appropriate for animals thatreproduce in a synchronous bout, many cooperative breeders produceoffspring over a prolonged period of time. It is likely thatthese species adjust reproductive allocation and group membershipover time in response to temporal shifts in group productivityand ecological constraints. In this paper we adapt transactionalmodels of reproductive skew to a continuous form, generatingtime-dependent functions of reproductive allocation. We derivea general method for predicting temporal changes in group membershipas well as a general expression for reproductive skew acrossthe regions over which a group is stable. Using a linear approximationfor time-dependent reproduction, we derive new expressions forreproductive skew in cases where the subordinate departs duringthe breeding period. In this case we find that the traditionalmodel always overestimates the subordinate's share of reproductionwhen dominants are in control of both reproductive shares andgroup membership (i.e., concessions models). Conversely, wefind that the traditional model always underestimates the subordinate'sshare of reproduction when subordinates are in control of reproductiveshares (i.e., constraint models). We discuss the implicationsof these new calculations in relation to the traditional skewmodels and more recent empirical tests of reproductive skewin animal societies.     

Higher reproductive skew among birds than mammals in cooperatively breeding species

While competition for limited breeding positions is a common feature of group life, species vary widely in the extent to which reproduction is shared among females (‘reproductive skew’). In recent years, there has been considerable debate over the mechanisms that generate variation in reproductive skew, with most evidence suggesting that subordinates breed when dominants are unable to prevent them from doing so. Here, we suggest that viviparity reduces the ability of dominant females to control subordinate reproduction and that, as a result, dominant female birds are more able than their mammal counterparts to prevent subordinates from breeding. Empirical data support this assertion. This perspective may increase our understanding of how cooperative groups form and are stabilized in nature.     

The evolution of parental and alloparental effort in cooperatively breeding groups: when should helpers pay to stay?

We used a reproductive skew framework to consider the evolutionof parental and alloparental effort in cooperatively breedinggroups. The model provides the first theoretical treatmentof rent payment (the "pay-to-stay" hypothesis) for the evolutionof helping behavior of subordinates. According to this hypothesis,not all helping behavior is kin selected, but group membershelp in order to be allowed to stay in the group and potentiallygain breeding positions later in life. We show that reproductiveconcessions may be replaced by complete skew and voluntary,costly alloparental effort by subordinates once future prospectsare included in fitness calculations. This suggests that incompleteskew observed in long-lived species is not due to dominantcontrol over reproduction. Rent payment is predicted to occurwhen relatedness between subordinate and dominant is low, survivalis high, ecological constraints are at least moderately tight,and retaining nonhelping subordinates harms the dominant'sfitness. Rent may also be required from related subordinatesif helping is very costly (leading to low voluntary helpingeffort) and ecological constraints are moderately tight. However, related subordinates do not need to have a positive net effecton the dominant's direct fitness to be accepted as group members.We also consider compensatory responses of dominant group membersas a potential threat to the stability of renting behavior.If dominants trade off parental effort against their own survival,they may selfishly reduce their own parental effort as a responseto increased help. As this improves their own survival, theprospects of territorial inheritance diminish for the subordinate,and subordinates should hence be less willing to accept therent agreement. However, we show that compensatory responsesby "lazy" parents prevent group formation only in borderlinecases.     

Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups

By living in social groups with potential competitors, animals forgo monopolizing access to resources. Consequently, debate continues over how selection might favour sociality among competitors. For example, several models exist to account for the evolution of shared reproduction in groups. The 'concession model' hypothesizes that dominant reproducers benefit from the presence of subordinates, and hence tolerate some reproduction by subordinates. This mutual benefit to both dominants and subordinates may provide a foundation for the formation of social groups in which multiple members reproduce-a necessary step in the evolution of cooperation. To date, however, the concession model has received virtually no support in vertebrates. Instead, the vast majority of vertebrate data support 'limited control models', which posit that dominant reproducers are simply unable to prevent subordinates from reproducing. Here we present the most comprehensive evidence to date in support of the concession model in a vertebrate. We examined natural variation in the number of adult males in gelada (Theropithecus gelada) reproductive units to assess the extent of reproductive skew in multi-male units. Dominant ('leader') males in units that also had subordinate ('follower') males had a 30 per cent longer tenure than leaders in units that did not have followers, mainly because followers actively defended the group against potential immigrants. Follower males also obtained a small amount of reproduction in the unit, which may have functioned as a concession in return for defending the unit. These results suggest that dominants and subordinates may engage in mutually beneficial reproductive transactions, thus favouring male-male tolerance and cooperation.     

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.     

Reproductive skew in cooperative breeding: Environmental variability,antagonistic selection,choice, and control

A multitude of factors may determine reproductive skew among cooperative breeders. One explanation, derived from inclusive fitness theory, is that groups can partition reproduction such that subordinates do at least as well as noncooperative solitary individuals. The majority of recent data, however, fails to support this prediction; possibly because inclusive fitness models cannot easily incorporate multiple factors simultaneously to predict skew. Notable omissions are antagonistic selection (across generations, genes will be in both dominant and subordinate bodies), constraints on the number of sites suitable for successful reproduction, choice in which group an individual might join, and within‐group control or suppression of competition. All of these factors and more are explored through agent‐based evolutionary simulations. The results suggest the primary drivers for the initial evolution of cooperative breeding may be a combination of limited suitable sites, choice across those sites, and parental manipulation of offspring into helping roles. Antagonistic selection may be important when subordinates are more frequent than dominants. Kinship matters, but its main effect may be in offspring being available for manipulation while unrelated individuals are not. The greater flexibility of evolutionary simulations allows the incorporation of species‐specific life histories and ecological constraints to better predict sociobiology.     

Reproductive skew in birds: models, problems and prospects

In recent years there has been a resurgence of interest in models to explain the partitioning of direct reproduction ('reproductive skew') among members of one sex within social groups. We review models of skew, identify problems of testing models, and consider how to make progress. One series of models assumes that dominants have complete control of subordinate reproduction, but may allow subordinates some reproduction as a way of enticing them to help or getting them to share the cost of reproduction. Another series of models assume that dominants have limited control of subordinate reproduction. Reproductive skew may also be affected by incest avoidance or control by the opposite sex. Models are largely untested because no study of birds has quantified all relevant parameters, and we see no prospect of this happening soon. A common simplifying approach is to test qualitative predictions about the effect on skew of relatedness among group members. However, these data alone cannot distinguish among models because models do not make unique predictions, partly because skew is also affected by other factors. A major problem in cooperatively-breeding birds is that any effect of relatedness will often be confounded by covariation with relatedness asymmetry and subordinate competitiveness. Progress can be made with the development of theory, controlling confounding variables through the choice of study species or types of social group, and, most importantly, testing assumptions underlying hypotheses.     

Sex differences in the drivers of reproductive skew in a cooperative breeder

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high‐skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long‐term genetic and observational data to examine factors affecting reproductive skew in the high‐skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within‐group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate‐guarding and potentially reproductive restraint (for males). Ecological conditions or “outside options” affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.     

Reproductive skew and indiscriminate infanticide

In communally breeding animals, there is an evolutionary conflict over the partitioning of reproduction within the group. If dominant group members do not have complete control over subordinate reproduction, this conflict may favour the evolution of infanticidal behaviour (by either subordinates or dominants or both). Elimination of offspring, however, is likely to be constrained by the difficulty of discriminating between an individual's own progeny and those of cobreeders. Here, we develop an evolutionarily stable strategy (ESS) model of reproductive partitioning, which demonstrates that killing of young can be favoured, even if such discrimination is not possible. The model predicts that infanticide will typically be associated with elevated levels of offspring production, and is most likely to prove evolutionarily stable when the coefficient of relatedness between cobreeders is low, and offspring are cheap to produce. The effect of infanticide is to release subordinates from the reproductive restraint they would otherwise be forced to exercise, leading to reduced reproductive skew. When infanticide is possible, addition of numerous young to the joint brood will not lower overall productivity, because progeny in excess of the most productive brood size are eliminated. Subordinates are thus free to contribute more young to the brood than would otherwise be the case. In addition, we show that the possibility of infanticide may influence the pattern of reproduction within a group even if no offspring are actually killed at equilibrium. Copyright 1999 The Association for the Study of Animal Behaviour.     

The causes of physiological suppression among female meerkats: a role for subordinate restraint due to the threat of infanticide?

In many animal societies, subordinates exhibit down-regulated reproductive endocrine axes relative to those of dominants, but whether this 'physiological suppression' arises from active interference by dominants or subordinate self-restraint is a matter of debate. Here we investigate the roles that these processes play in precipitating physiological suppression among subordinate female meerkats, Suricata suricatta. We show that, while subordinate females are known to suffer stress-related physiological suppression during periodic temporary evictions by the dominant female, their low estrogen levels while within their groups cannot be readily attributed to chronic stress, as their fecal glucocorticoid metabolite levels during this time are comparable to those of dominants. The low estrogen levels of subordinate females also cannot be explained simply by self-restraint due to factors that could reduce their payoff from maintaining their fertility regardless of the presence of the dominant female (young age, a lack of unrelated mates, poor body condition and limited breeding experience), as substantial rank-related differences in fecal total-estrogen metabolite levels remain when such factors are controlled. We suggest that this residual difference in estrogen levels may reflect a degree of subordinate restraint due in part to the dominant female's ability to kill their young. Accordingly, subordinate female estrogen levels vary in association with temporal variation in the likelihood of infanticide by the dominant. Attempts to identify the causes of physiological suppression should be cautious if rejecting any role for dominant interference in favor of subordinate restraint, as the dominant's capacity to interfere may often be the reason why subordinates exercise restraint.     

Are reproductive skew models evolutionarily stable?

Reproductive skew theory has become a popular way to phrase problems and test hypotheses of social evolution. The diversity of reproductive skew models probably stems from the ease of generating new variations. However, I show that the logical basis of skew models, that is, the way in which group formation is modelled, makes use of hidden assumptions that may be problematical as they are unlikely to be fulfilled in all social systems. I illustrate these problems by re-analysing the basic concessive skew model with staying incentives. First, the model assumes that dispersal is an all-or-nothing response: all subordinates disperse as soon as concessions drop below a certain value. This leads to a discontinuous 'cliff-edge' shape of dominant fitness, and it is not clear that selection will balance a population at such an edge. Second, it is assumed that subordinates have perfect knowledge of their benefits if they stay in the group. I examine the effects of relaxing these two assumptions. Relaxing the first one strengthens reproductive skew theory, but relaxing the latter makes evolutionary stability disappear. In cases where subordinates cannot accurately measure benefits provided by the individual dominant with which they live, so that their behaviour instead evolves as a response to population-wide average benefits, the logic of reproductive skew models does not apply. This warns against too indiscriminate an application of reproductive skew theory to problems in social evolution: for example, transactional models of extra-pair paternity assume perfect knowledge of paternity, which is unlikely to hold true in nature. It is recommended that models specify the mechanisms by which individuals can adjust their behaviour to that of others, and pay attention to changes that occur in evolutionary versus behavioural time.     

Reproductive skew, costs, and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus)

Two current models seek to explain reproduction of subordinatesin social groups: incentives given by dominants for peacefullyremaining in the group (reproductive skew model) or incompletecontrol by dominants. These models make different predictionsconcerning genetic relatedness between individuals for thedistribution of reproduction and the stability of cooperativebreeding associations. To test these models and to furtherexplore the relationships between reproductive skew, geneticrelatedness, and investment of each participant, we performedbehavioral observations of female wood mice (Apodemus sylvaticus)raising pups communally. Our results do not support previousmodels. Differences in lifetime reproductive success were significantlygreater within mother—daughter pairs than within pairsof sisters or unrelated females. Subordinate females of eitherbreeding unit did not differ in their direct reproduction.Calculations of inclusive fitness based on our results leadto the following predictions: (1) Communal nests should occuronly when ecological circumstances prevent solitary breeding.(2) Subordinate females gain the highest inclusive fitnessjoining their mothers; they also show the highest nursing investment.(3) Mothers should accept daughters, who have no opportunityfor solitary breeding. (4) Dominant sisters and unrelated femalesshould reject subordinate females because cooperative breedingreduces their reproductive success. However, breeding unitsof dominant sisters and unrelated females nevertheless occurand can be explained by our finding that such females significantlyreduce nursing time, which may help them save energy for futurebreeding cycles. Our data demonstrate that both genetic relatednessand investment skew are important in the complex evolutionof reproductive skew in cooperative breeding.