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.     

Reproductive skew and group size: an N-person staying incentive model

Transactional models of social evolution emphasize that dominantbreeders may donate parcels of reproduction to subordinatesin return for peaceful cooperation. We develop a general transactionalmodel of reproductive partitioning and group size for N-persongroups when (1) expected group output is a concave (decelerating)functiong[N] of the number N of group members, and (2) thesubordinates may receive fractions of total group reproduction("staying incentives") just sufficient to induce them to stayand help the dominant instead of breeding solitarily. We focusespecially on "saturated" groups, that is, groups that havegrown in size just up to the point where subsequent joining by subordinates is no longer beneficial either to them (in parent-offspring groups) or to the dominant (in symmetric-relatedness groups).Decreased expected output for solitary breeding increases thesaturated group size and decreases the staying incentives.Increased relatedness decreases both the saturated group sizeand the staying incentives. However, in saturated groups withsymmetric relatedness, an individual subordinate's staying incentive converges to 1 — g[N^* — 1]/g[N^*]) regardless ofrelatedness, where N^* is the size of a saturated group, providedthat the g[N] function near the saturated group size N^* isapproximately linear. Thus, staying incentives can be insensitiveto relatedness in saturated groups, although the dominant's total fraction of reproduction (total skew) will be more sensitive.The predicted ordering for saturated group size is: Parent-fullsibling offspring = non-relatives > symmetrically relatedrelatives. Strikingly, stable groups of non-relatives can formfor concaveg[N] functions in our model but not in previousmodels of group size lacking skew manipulation by the dominant.Finally, symmetrical relatedness groups should tend to breakup by threatened ejections of subordinates by dominants, whereas parent-offspring groups should tend to breakup via unforceddepartures by subordinates.     

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.     

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.     

Within‐group relatedness is correlated with colony‐level social structure and reproductive sharing in a social fish

In group‐living species, the degree of relatedness among group members often governs the extent of reproductive sharing, cooperation and conflict within a group. Kinship among group members can be shaped by the presence and location of neighbouring groups, as these provide dispersal or mating opportunities that can dilute kinship among current group members. Here, we assessed how within‐group relatedness varies with the density and position of neighbouring social groups in Neolamprologus pulcher, a colonial and group‐living cichlid fish. We used restriction site‐associated DNA sequencing (RADseq) methods to generate thousands of polymorphic SNPs. Relative to microsatellite data, RADseq data provided much tighter confidence intervals around our relatedness estimates. These data allowed us to document novel patterns of relatedness in relation to colony‐level social structure. First, the density of neighbouring groups was negatively correlated with relatedness between subordinates and dominant females within a group, but no such patterns were observed between subordinates and dominant males. Second, subordinates at the colony edge were less related to dominant males in their group than subordinates in the colony centre, suggesting a shorter breeding tenure for dominant males at the colony edge. Finally, subordinates who were closely related to their same‐sex dominant were more likely to reproduce, supporting some restraint models of reproductive skew. Collectively, these results demonstrate that within‐group relatedness is influenced by the broader social context, and variation between groups in the degree of relatedness between dominants and subordinates can be explained by both patterns of reproductive sharing and the nature of the social landscape.     

A genetic analysis of breeding success in the cooperative meerkat (Suricata suricatta)

Measurement of reproductive skew in social groups is fundamentalto understanding the evolution and maintenance of sociality,as it determines the immediate fitness benefits to helpers ofstaying and helping in a group. However, there is a lack ofstudies in natural populations that provide reliable measuresof reproductive skew and the correlates of reproductive success,particularly in vertebrates. We present results of a study thatuses a combination of field and genetic (microsatellite) dataon a cooperatively breeding mongoose, the meerkat (Suricatasuricatta). We sampled 458 individuals from 16 groups at twosites and analyzed parentage of pups in 110 litters with upto 12 microsatellites. We show that there is strong reproductiveskew in favor of dominants, but that the extent of skew differsbetween the sexes and between different sites. Our data suggestthat the reproductive skew arises from incest avoidance andreproductive suppression of the subordinates by the dominants.     

Colony genetic structure in a facultatively eusocial hover wasp

The degree of genetic heterogeneity among the individuals inan animal society depends on the society's genetic structure.Genetic heterogeneity, in turn, means that group members willdiffer in their reproductive objectives and conflicts over reproductionmay arise. The resolution of these conflicts may be reflectedin the way that reproduction is partitioned between potentialreproductives. We used 5 microsatellite loci to investigategenetic structure and reproductive skew in 17 nests of the Malaysianhover wasp, Parischnogaster alternata. Parischnogaster alternatacolonies are small (1–10 females), and all adult colonymembers are capable of mating and producing offspring. We foundthat colonies tended to consist of closely related individualsand that at any one time the production of both female and maleoffspring was nearly always monopolized by a single dominantfemale, despite considerable variation between nests in parameterspredicted to affect skew. Subordinate females that remainedin their natal colonies obtained indirect fitness benefits byhelping to raise offspring to which they were related. Subordinatefemales also appeared to be positioned within an age-based queuefor inheritance of the dominant egg-laying position. We suggestthat the high skew in P. alternata may result from strong ecologicalconstraints on solitary nesting, high relatedness, and a relativelyhigh probability that subordinates will eventually inherit theposition of dominance.     

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.     

A skew model for the evolution of sociality via manipulation: why it is better to be feared than loved

Concession-based reproductive skew models predict that social groups can form via persuasion, whereby dominant individuals forfeit some reproduction to subordinates as an incentive to stay and help. We have developed an alternative skew model based on manipulation, whereby dominant individuals coerce subordinates into staying and helping by imposing costs on their independent reproductive prospects. Stable groups can evolve under a much wider range of genetic and ecological conditions under this manipulation model than under concession models. We describe evidence that various forms of pre-emptive and ongoing manipulation occur in nature and we discuss the implications of the model for the development of a general theory of social evolution.     

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.     

Reproductive skew and the origin of sterile castes

Reproductive skew theory has not heretofore formally addressed one of the most important questions in evolutionary biology: How can whole-life sterile castes evolve? We construct a transactional skew model investigating under what conditions a subordinate in a multimember group is favored to develop into a morphologically specialized worker caste. Our model demonstrates that, contrary to former expectations, the ecological and genetic conditions favoring caste differentiation are far more restrictive than those favoring high skew. Caste differentiation cannot be selected in saturated, symmetrical relatedness groups unless the genetic relatedness among group members is extremely high. In contrast, it can be selected in the saturated, asymmetrical relatedness (parent-offspring) groups with complete skew. If we also consider the future reproduction of subordinates, caste differentiation is possible only after the group size reaches a certain critical point. Most importantly, caste differentiation in a parent-offspring group increases its saturated group size. The positive feedback between group size and the degree of caste differentiation can continue in principle until completely sterile worker castes emerge. Thus, at least in the case of parent-offspring groups, group size but not the degree of reproductive skew may be a better index of the level of social complexity. A scheme for the evolution of sterile worker castes that integrates the role of group size into the framework of reproductive skew theory is proposed.     

Social and genetic structure of paper wasp cofoundress associations: tests of reproductive skew models

Recent models postulate that the members of a social group assess their ecological and social environments and agree a "social contract" of reproductive partitioning (skew). We tested social contracts theory by using DNA microsatellites to measure skew in 24 cofoundress associations of paper wasps, Polistes bellicosus. In contrast to theoretical predictions, there was little variation in cofoundress relatedness, and relatedness either did not predict skew or was negatively correlated with it; the dominant/subordinate size ratio, assumed to reflect relative fighting ability, did not predict skew; and high skew was associated with decreased aggression by the rank 2 subordinate toward the dominant. High skew was associated with increased group size. A difficulty with measuring skew in real systems is the frequent changes in group composition that commonly occur in social animals. In P. bellicosus, 61% of egg layers and an unknown number of non-egg layers were absent by the time nests were collected. The social contracts models provide an attractive general framework linking genetics, ecology, and behavior, but there have been few direct tests of their predictions. We question assumptions underlying the models and suggest directions for future research.     

From individual control to majority rule: extending transactional models of reproductive skew in animal societies

Transactional concession models of social evolution explain the reproductive skew within groups by assuming that a dominant individual completely controls the allocation of reproduction to other group members. The models predict when the dominant will benefit from donating parcels of reproduction to other members in return for peaceful cooperation. Using linear programming methods, we present a 'majority-rules' model in which the summed actions of all society members, each with equal power, completely determine the reproductive share of any single member. The majority-rules model predicts that, despite the diffusion of power, a 'virtual dominant' (a dominant lacking special behavioural power) will emerge and that the reproductive skew will be exactly that predicted if the virtual dominant were to control completely the group's reproductive partitioning. The virtual dominant is the individual to which group members have the maximum average genetic relatedness. This result greatly broadens the applicability of transactional models of reproductive skew to social groups of any size, such as large-colony eusocial insects, and explains why queens in such colonies can achieve reproductive domination without any behavioural enforcement. Moreover, the majority-rules model unifies transactional-skew theory with models of worker policing and even generates a new theory for the cooperation among somatic cells in a multicellular organism.     

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.     

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.     

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.     

Reproduction in foundress associations of the social wasp, Polistes carolina: conventions, competition, and skew

Who reproduces in colonies of social insects is determined bysome combination of direct competition and more peaceful convention.We studied these two alternatives in foundresses of the paperwasp, Polistes carolina, by examining two different contexts:what determines who becomes the dominant reproductive and whatdetermines the amount of reproduction obtained by subordinates.The dominant queen on most nests was the foundress to arrivefirst, rather than the largest foundress, expected to be bestat fighting. This suggests that dominance is initially determinedby convention, although the persistence of some aggressiveconflict throughout the foundress period suggests that thisconvention is not absolute. Attempts to explain the divisionof reproduction using several skew theories were generallyunsuccessful. Skew was not correlated with relatedness, size differences, colony productivity, and challenges by the subordinate.P. carolina showed high constraints against solitary nesting,with a minority of females attempting to nest alone, and nonesucceeding. In this situation, most skew theories predict thatgroup stability will be independent of relatedness, yet nearlyall collected subordinates were full sisters to the queen.Reproductive partitioning in early P. carolina colonies may have more to do with enhancing worker production than with conflictover direct fitness.     

Power Struggles, Dominance Testing, and Reproductive Skew

Models of reproductive skew are concerned with the partitioning of reproduction between dominant and subordinate members of a group. In an interesting extension of these models, Reeve and Ratnieks briefly considered whether it might benefit subordinates to engage in aggressive behavior to test the fighting ability of a dominant. Their analysis suggested that such testing should be more probable in groups that feature high skew and, hence, perhaps among closer relatives (because high relatedness favors high skew). Here we explore in more detail the possibility of dominance testing. Three models that differ in the outcome of fights over dominance are presented: in the first model, the loser of the challenge is killed; in the second model, the loser is evicted from the nest; and, in the third model, the loser becomes (or remains) subordinate. In each case we consider the independent effects of the parameters that determine skew (namely, relatedness, group productivity, and ecological constraints) on the predicted level of dominance testing. We then construct an amalgamated model to examine situations where fights may lead to any one of the three outcomes. Our analysis reveals that, in the majority of cases, higher relatedness will in fact lead to lower levels of aggression. Moreover, dominance testing need not be associated with high skew. Rather, the relationship between skew and dominance testing will depend on which factor (relatedness, group productivity, or level of ecological constraints) is principally responsible for variation in the distribution of reproduction.     

Sex ratios and skew models: the special case of evolution of cooperation in polistine wasps

Cooperative breeding often involves reproductive dominance hierarchies. Such hierarchies have been proposed to form and to be maintained through an equitable skew in reproduction for both dominants and subordinates. The general form of skew models also predicts that cooperation can be stable only if cooperation greatly increases group reproductive success or subordinates are greatly constrained in their reproductive prospects relative to dominants. Neither, however, seems to be generally present in the colony initiation phase of temperate polistine wasps, although the behaviors of individuals within such groups are often consistent with skew model predictions. This apparent contradiction can be resolved in the context of a special case of the skew models that incorporate mother-offspring conflicts over sex ratios. Data suggest that all the needed preconditions are present for cooperating foundresses to gain an added benefit through producing male-biased investment ratios. Therefore, the special case model predicts that cooperation can evolve in Hymenoptera with both the observed high skews and reduced per capita group productivity. Further predictions of the special case model (e.g., mixed populations of single and multifoundresses) are also supported. Because the special case model is applicable only to haplodiploids, this may explain why cooperation in vertebrates rarely occurs without significant ecological or physiological constraints. Finally, comparisons to other social Hymenoptera taxa suggest that factors stabilizing cooperation between colony-initiating females may simultaneously constrain the evolution of morphologically specialized worker castes.