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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

A Model of Mutual Tolerance and the Origin of Communal Associations Between Unrelated Females

We use a genetic algorithm model employing game theory to explore the ecological conditions favoring reproductive tolerance between two unrelated females that meet at a nesting site (i.e., breeding resource). Each female adopts one of three strategies: (1) fight for exclusive use of the nest, (2) tolerate the other female and breed communally, but fight back if attacked, or (3) leave in search of new breeding opportunities. Nests vary in the number of offspring they can support and their probability of failure due to discovery by competitors. The model predicts that communal associations are most likely to arise when (1) the benefits of nest sharing to females exceed the losses to individual reproduction, (2) additional nesting sites are rare, (3) females have limited clutch sizes, and (4) dominant females are able to skew reproduction in their favor. The amount of reproductive skew a dominant (larger) female can acquire while maintaining a communal association is predicted to increase when the asymmetry in fighting ability between females increases, and at nests that have a relatively high probability of nesting success for solitary females. When the losers of fights can parasitize the winner's brood, dominant females must reduce reproductive skew to promote a communal relationship. We discuss the ability of our model to predict patterns of facultative communal behavior in burying beetles (Silphidae; Nicrophorus spp.), as well as the absence of communal behavior in dung beetles (Scarabaeidae).     

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.     

Cichlids do not adjust reproductive skew to the availability of independent breeding options

Helpers in cooperatively breeding species forego all or partof their reproduction when remaining at home and assisting breedersto raise offspring. Different models of reproductive skew generatealternative predictions about the share of reproduction unrelatedsubordinates will get depending on the degree of ecologicalconstraints. Concession models predict a larger share when independentbreeding options are good, whereas restraint and tug-of-warmodels predict no effects on reproductive skew. We tested thesepredictions by determining the share of reproduction by unrelatedmale and female helpers in the Lake Tanganyika cichlid Neolamprologuspulcher depending on experimentally manipulated possibilitiesfor helper dispersal and independent breeding and dependingon helper size and sex. We created 32 breeding groups in thelaboratory, consisting of two breeders and two helpers each,where only the helpers had access to a nearby dispersal compartmentwith (treatment) or without (control) breeding substrate, usinga repeated measures design. We determined the paternity andmaternity of 1185 offspring from 47 broods using five to nineDNA microsatellite loci and found that: (1) helpers participatedin reproduction equally across the treatments, (2) large malehelpers were significantly more likely to reproduce than smallhelpers, and (3) male helpers engaged in significantly morereproduction than female helpers. Interestingly, in four broods,extragroup helper males had fertilized part of the brood. Nohelper evictions from the group after helper reproduction wereobserved. Our results suggest that tug-of-war models based oncompetition over reproduction within groups describe best thereproductive skew observed in our study system. Female breedersproduced larger clutches in the treatment compared to the controlsituation when the large helpers were males. This suggests thatmale breeder-male helper reproductive conflicts may be alleviatedby females producing larger clutches with helpers around.     

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.     

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.     

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.     

Tug-of-war has no borders: it is the missing model in reproductive skew theory

Cooperative breeding often results in unequal reproduction between dominant and subordinate group members. Transactional skew models attempt to predict how unequal reproduction can be before the groups themselves become unstable. A number of variants of transactional models have been developed, with a key difference being whether reproduction is controlled by one party or contested by all. It is shown here that ESS solutions for all situations of contested control over reproduction are given by the original tug-of-war model (TOW). Several interesting results follow. First, TOW can escalate enough to destabilize some types of groups. Particularly vulnerable are those that have low relatedness and gain little from cooperative breeding relative to solitary reproduction. Second, TOW can drastically reduce group productivity and especially the inclusive fitness of dominant individuals. Third, these results contrast strongly with those from variants of TOW models that include concessions to maintain group stability. Such models are shown to be special cases of the general and simpler TOW framework, and to have assumptions that may be biologically suspect. Finally, the overall analysis suggests that there is no mechanism within existing TOW framework that will prevent a costly struggle for reproductive control. Because social species rarely exhibit the high levels of aggression predicted by TOW models, alternative evolutionary mechanisms are considered that can limit conflict and produce more mutually beneficial outcomes. The further development of alternative models to predict patterns of reproductive skew are highly recommended.     

Male-caused failure of female reproduction and its adaptive value in alpine marmots (Marmota marmota)

We studied reproductive performance of free-living alpine marmots (Marmotamarmota) for 14 years in the National Park of Berchtesgaden, Germany.Female reproduction was influenced by body condition and social factors.Reproduction depleted fat reserves, and only females emergingfrom hibernation with sufficient body mass were able to reproducesuccessfully. Marmots lived in social groups in territoriesdefended by a dominant male and female. Subordinate femalesnever reproduced, regardless of body mass. Territory takeoversby males impaired reproduction of dominant females, but onlyif the takeover occurred after the mating period. Reproductivefailures occurred despite clear signs of pregnancy such enlargednipples or late molt. Decreasing progesterone levels after themating period and the lack of evidence for direct infanticideby new territorial males suggest a block of pregnancy as a likelyexplanation for reproductive failures in groups with male takeoversduring gestation. Rendering female reproduction impossible increasedfuture reproductive success of new territory owners. Nonparous femalessaved the energetic cost of maternal investment and thus emergedwith higher body mass in the following spring. In line withthis, females failing to wean young had higher reproductivesuccess in the subsequent year.     

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo‐maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet‐hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini‐meta‐analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet‐hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.     

Costly reproductive competition between females in a monogamous cooperatively breeding bird

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding 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.     

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.