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.     

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 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 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.     

Dominance, reproduction and survival in banded mongooses: towards an egalitarian social system?

The banded mongoose, Mungos mungo, is a social species that forms multimale and multifemale family groups. Earlier studies suggest these family groups are relatively egalitarian with small differences in reproductive opportunities among individuals of different rank. In contrast, previous studies of other social mongooses have focused on species with more despotic control of reproduction (meerkats, Suricata suricatta, dwarf mongooses, Helogale parvula). In these species, the distribution of reproductive opportunities amongst individuals of different rank has met the predictions of reproductive skew theory: dominant individuals accrue greater reproductive benefits than subordinates, with subordinates breeding less often than dominants. In this paper we test how well two predictions of reproductive skew theory explain variance in measures of reproductive effort, and its correlates, in a wild population of banded mongooses in Queen Elizabeth National Park, Uganda. We measure dominance rank in males and females, and we investigate whether individuals of higher social rank accrue greater benefits than subordinates in terms of survival and reproduction. Banded mongoose dominance hierarchies showed linearity, but low reproductive skew. Rank was not significantly correlated with age. Furthermore, there were only small effects of dominance rank on nutritional levels, and no effects on reproduction and survival, suggesting that banded mongoose societies are indeed relatively egalitarian. No evidence of reproductive suppression was found and other forms of reproductive control were not observed. However, we do not exclude the possibility of increased reproductive competition in circumstances of higher ecological constraints. These findings show that reproductive skew theory is equally useful in explaining variation in reproduction in societies with low reproductive skew, as it is in explaining the allocation of reproductive effort in despotic social systems. Copyright 2001 The Association for the Study of Animal Behaviour.     

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 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.     

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.     

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.     

Reproductive skew can provide a net advantage in both conditional and unconditional social interactions

We revisit a model for the evolution of costly social behaviour in the presence of reproductive skew. The model population is structured into groups, and reproductive skew is captured by assuming individuals adopt one of two social roles (dominant/subordinate). Unlike previous work, we adopt an ultimate perspective by tracking a mutant allele over the entire course of an invasion. Our main analysis applies the theory of branching processes, but a parallel analysis using the inclusive-fitness approach is also provided. Our first two results are modifications of known inequalities describing selective advantages for behaviours expressed conditional upon social status. We find that altruistic subordinate individuals are favoured more readily than previously thought; spiteful dominant individuals, however, are favoured less readily. Secondly, we identify the condition under which unconditional altruism (performed by both dominant and subordinate) will be adaptive. Our third main result shows that increasing the strength of selection can also change the range of parameters over which costly social behaviours are favoured. We find that stronger selection makes it relatively easier for subordinate altruism to emerge, but more difficult for dominant spite and unconditional altruism to occur. We discuss the possible implications of our results for human social evolution.     

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.     

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.     

Inbreeding avoidance and reproductive skew in a cooperative mammal

In animal social groups, socially subordinate individuals frequently show low reproductive success or completely fail to breed. This suppression of subordinate reproduction is currently typically attributed to control by dominant individuals. However, subordinates in cooperative groups often lack access to unrelated mates, and an alternative possibility is that their reproduction is limited by inbreeding avoidance. Using the eusocial Damaraland mole-rat Cryptomys damarensis, this paper provides the first experimental evidence, to our knowledge, for this explanation. Subordinate, non-breeding female mole-rats were given access to unrelated mates while remaining in the presence of dominant females, and many became reproductively active soon after unrelated males were introduced. Inbreeding avoidance and the availability of unrelated mates provides a plausible and untested explanation for variation in reproductive skew across animal societies.     

Using social parasitism to test reproductive skew models in a primitively eusocial wasp

Remarkable variation exists in the distribution of reproduction (skew) among members of cooperatively breeding groups, both within and between species. Reproductive skew theory has provided an important framework for understanding this variation. In the primitively eusocial Hymenoptera, two models have been routinely tested: concessions models, which assume complete control of reproduction by a dominant individual, and tug-of-war models, which assume on-going competition among group members over reproduction. Current data provide little support for either model, but uncertainty about the ability of individuals to detect genetic relatedness and difficulties in identifying traits conferring competitive ability mean that the relative importance of concessions versus tug-of-war remains unresolved. Here, we suggest that the use of social parasitism to generate meaningful variation in key social variables represents a valuable opportunity to explore the mechanisms underpinning reproductive skew within the social Hymenoptera. We present a direct test of concessions and tug-of-war models in the paper wasp Polistes dominulus by exploiting pronounced changes in relatedness and power structures that occur following replacement of the dominant by a congeneric social parasite. Comparisons of skew in parasitized and unparasitized colonies are consistent with a tug-of-war over reproduction within P. dominulus groups, but provide no evidence for reproductive concessions.     

Optimal reproductive-skew models fail to predict aggression in wasps

Optimal-skew models (OSMs) predict that cooperative breeding occurs as a result of dominants conceding reproductive benefits to subordinates, and that division of reproduction within groups reflects each cooperator's willingness and ability to contest aggressively for dominance. Polistine paper wasps are a leading model system for testing OSMs, and data on reproduction and aggression appear to support OSMs. These studies, however, measure aggression as a single rate rather than by the activity patterns of individuals. This leads to a potential error: if individuals are more likely to receive aggression when active than when inactive, differences in aggression across samples can reflect changes in activity rather than hostility. This study replicates a field manipulation cited as strongly supporting OSMs. We show that fundamentally different conclusions arise when controlling for individual activity states. Our analyses strongly suggest that behaviours classified as 'aggression' in paper wasps are unlikely to function in establishing, maintaining or responding to changes in reproductive skew. This illustrates that OSM tests using aggression or other non-reproductive behaviour as a metric for reproductive partitioning must demonstrate those links rather than assume them.     

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.     

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.     

The relative influence of prior residency and dominance on the early feeding behaviour of juvenile Atlantic salmon

In many species where social hierarchy mediates conflict over resources, dominant individuals monopolize food, shelter and reproductive opportunities. The benefits of social dominance, however, can often be offset by a prior residence advantage, whereby individuals arriving first in a new habitat obtain, and subsequently defend, the most profitable sites. We investigated the relative influence of these two factors on the acquisition of feeding territories by juvenile Atlantic salmon,Salmo salar L., by placing groups of six individuals of known dominance rank sequentially into an experimental arena with feeding sites of varying quality. Dominants had an advantage over subordinates in the percentage of time spent in a good-quality feeding site and individual feeding rate. There was also a significant time of arrival effect: those individuals that arrived first in a habitat monopolized the resource. The two effects were of approximately equal strength, so that late-arriving dominant fish had similar success as prior resident subordinates. These results indicate that both dominance and prior residence are important in the feeding behaviour of juvenile Atlantic salmon, and that the two factors can have independent and additive effects.Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

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.     

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.