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The origin of eusociality in the Hymenoptera is a question of major interest. Theory has tended to focus on genetic relatedness, but ecology can be just as important a determinant of whether eusociality evolves. Using the model of Fu et al. (2015), we show how ecological assumptions critically affect the conclusions drawn. Fu et al. inferred that eusociality rarely evolves because it faces a fundamental ‘risk‐return tradeoff’. The intuitive logic was that worker production represents an opportunity cost because it delays realising a reproductive payoff. However, making empirically justified assumptions that (1) workers take over egg‐laying following queen death and (2) productivity increases gradually with each additional worker, we find that the risk‐return tradeoff disappears. We then survey Hymenoptera with more specialised morphological castes, and show how the interaction between two common features of eusociality – saturating birth rates and group size‐dependent helping decisions – can determine whether eusociality outperforms other strategies., Theories concerning the origin of eusociality in Hymenoptera have tended to focus on genetic relatedness, but ecology can be just as important. With realistic ecological assumptions, we show that eusociality does not face a previously postulated ‘risk‐return tradeoff’. We find that the interaction between two common features of eusociality – birth rates that saturate at large group sizes, and group‐size dependent helping decisions – can instead determine whether eusociality outperforms other strategies.

Abstract In eusocial Hymenoptera, queens and their helper offspring should favour different sex investment ratios. Queens should prefer a 1:1 investment ratio, as they are equally related to offspring of both sexes (r = 0.5). In contrast, helpers should favour an investment ratio of 3:1 towards the production of female brood. This conflict arises because helpers are more closely related to full sisters (r = 0.75) than brothers (r = 0.25). However, helpers should invest relatively more in male brood if relatedness asymmetry within their colony is reduced. This can occur due to queen replacement after colony orphaning, multiple paternity and the presence of unrelated alien helpers. We analysed an unprecedentedly large number of colonies (n = 109) from a UK population of Lasioglossum malachurum, an obligate eusocial sweat bee, to tease apart the effects of these factors on colony-level investment ratios. We found that multiple paternity, unrelated alien helpers and colony orphaning were all common. Queen-right colonies invested relatively more in females than did orphaned colonies, producing a split sex ratio. However, investment ratios did not change due to multiple paternity or the presence of alien helpers, reducing inclusive fitness pay-offs for helpers. Queen control may also have been important: helpers rarely laid male eggs, and investment in female brood was lower when queens were large relative to their helpers. Genetic relatedness between helpers and the brood that they rear was 0.43 in one year and 0.37 in another year, suggesting that ecological benefits, as well as relatedness benefits, are necessary for the maintenance of helping behaviour. Significance statement How helping behaviour is maintained in eusocial species is a key topic in evolutionary biology. Colony-level sex investment ratio changes in response to relatedness asymmetries can dramatically influence inclusive fitness benefits for helpers in eusocial Hymenoptera. The extent to which helpers in primitively eusocial colonies can respond adaptively to different sources of variation in relatedness asymmetry is unclear. Using data from 109 colonies of the sweat bee Lasioglossum malachurum, we found that queen loss, but not multiple paternity or the presence of alien helpers, was correlated with colony sex investment ratios. Moreover, we quantified average helper-brood genetic relatedness to test whether it is higher than that predicted under solitary reproduction (r = 0.5). Values equal to and below r = 0.5 suggest that relatedness benefits alone cannot explain the maintenance of helping behaviour. Ecological benefits of group living and/or coercion must also contribute.

Abstract Insect parental care strategies are particularly diverse, and prolonged association between parents and offspring may be a key precursor to the evolution of complex social traits. Macroevolutionary patterns remain obscure, however, due to the few rigorous phylogenetic analyses. The subsocial sphecid wasps are a useful group in which to study parental care because of the diverse range of strategies they exhibit. These strategies range from placing a single prey item in a pre-existing cavity to mass provisioning a pre-built nest, through to complex progressive provisioning where a female feeds larvae in different nests simultaneously as they grow. We show that this diversity stems from multiple independent transitions between states. The strategies we focus on were previously thought of in terms of a stepping-stone model in which complexity increases during evolution, ending with progressive provisioning which is a likely precursor to eusociality. We find that evolution has not always followed this model: reverse transitions are common, and the ancestral state is the most flexible rather than the simplest strategy. Progressive provisioning has evolved several times independently, but transitions away from it appear rare. We discuss the possibility that ancestral plasticity has played a role in the evolution of extended parental care. Significance statement Parental care behaviour leads to prolonged associations between parents and offspring, which is thought to drive the evolution of social living. Despite the importance of insect parental care for shaping the evolution of sociality, relatively few studies have attempted to reconstruct how different strategies evolve in the insects. In this study, we use phylogenetic methods to reconstruct the evolution of the diverse parental care strategies exhibited by the subsocial digger wasps (Sphecidae). Contrary to expectations, we show that parental care in this group has not increased in complexity over evolutionary time. We find that the ancestral state is not the simplest, but may be the most flexible strategy. We suggest that this flexible ancestral strategy may have allowed rapid response to changing environmental conditions which might explain the diversity in parental care strategies that we see in the digger wasps today.

Understanding the ecological and environmental contexts in which eusociality can evolve is fundamental to elucidating its evolutionary origins. A sufficiently long active season is postulated to have been a key factor facilitating the transition to eusociality. Many primitively eusocial species exhibit an annual life cycle, which is thought to preclude the expression of eusociality where the active season is too short to produce successive worker and reproductive broods. However, few studies have attempted to test this idea experimentally. We investigated environmental constraints on the expression of eusociality in the obligate primitively eusocial sweat bee Lasioglossum malachurum, by transplanting nest foundresses from the south to the far north of the United Kingdom, far beyond the natural range of L. malachurum. We show that transplanted bees can exhibit eusociality, but that the short length of the season and harsher environmental conditions could preclude its successful expression. In one year, when foundresses were transplanted only after provisioning first brood (B1) offspring, workers emerged in the north and provisioned a second brood (B2) of reproductives. In another year, when foundresses were transplanted prior to B1 being provisioned, they were just as likely to initiate nesting and provisioned just as many B1 cells as foundresses in the south. However, the life cycle was delayed by approximately 7 weeks and nests suffered 100% B1 mortality. Our results suggest that short season length together with poor weather conditions represent an environmental barrier to the evolution and expression of eusociality in sweat bees. Electronic supplementary material The online version of this article (10.1007/s00040-018-0642-7) contains supplementary material, which is available to authorized users.

The breeding and non-breeding 'castes' of eusocial insects provide a striking example of role-specific selection, where each caste maximises fitness through different morphological, behavioural and physiological trait values. Typically, queens are long-lived egg-layers, while workers are short-lived, largely sterile foragers. Remarkably, the two castes are nevertheless produced by the same genome. The existence of inter-caste genetic correlations is a neglected consequence of this shared genome, potentially hindering the evolution of caste dimorphism: alleles that increase the productivity of queens may decrease the productivity of workers and vice versa, such that each caste is prevented from reaching optimal trait values. A likely consequence of this 'intralocus caste antagonism' should be the maintenance of genetic variation for fitness and maladaptation within castes (termed 'caste load'), analogous to the result of intralocus sexual antagonism. The aim of this review is to create a research framework for understanding caste antagonism, drawing in part upon conceptual similarities with sexual antagonism. By reviewing both the social insect and sexual antagonism literature, we highlight the current empirical evidence for caste antagonism, discuss social systems of interest, how antagonism might be resolved, and challenges for future research. We also introduce the idea that sexual and caste antagonism could interact, creating a three-way antagonism over gene expression. This includes unpacking the implications of haplodiploidy for the outcome of this complex interaction.

Cooperation among kin is common in animal societies. Kin groups may form by individuals directly discriminating relatives based on kin recognition cues, or form passively through natal philopatry and limited dispersal. We describe the genetic landscape for a primitively eusocial wasp, Polistes dominula, and ask whether individuals choose cooperative partners that are nearby and/or that are genetic relatives. Firstly, we genotyped an entire sub-population of 1361 wasps and found genetic structuring on an extremely fine scale: the probability of finding genetic relatives decreases exponentially within just a few meters of an individual’s nest. At the same time, however, we found a lack of genetic structuring between natural nest aggregations within the population. Secondly, in a separate dataset where ~2000 wasps were genotyped, we show that wasps forced experimentally to make a new nest choice tended to choose new nests near to their original nests, and that these nests tended to contain some full sisters. However, a significant fraction of wasps chose nests that did not contain sisters, despite sisters being present in nearby nests. Although we cannot rule out a role for direct kin recognition or natal nest-mate recognition, our data suggest that kin groups may form via a philopatric rule-of-thumb, whereby wasps simply select groups and nesting sites that are nearby. The result is that most subordinate helpers obtain indirect fitness benefits by breeding cooperatively.

Eusociality is characterised by a reproductive division of labour, where some individuals forgo direct reproduction to instead help raise kin. Socially polymorphic sweat bees are ideal models for addressing the mechanisms underlying the transition from solitary living to eusociality, because different individuals in the same species can express either eusocial or solitary behaviour. A key question is whether alternative social phenotypes represent environmentally induced plasticity or predominantly genetic differentiation between populations. In this paper, we focus on the sweat bee Lasioglossum calceatum, in which northern or high-altitude populations are solitary, whereas more southern or low-altitude populations are typically eusocial. To test whether social phenotype responds to local environmental cues, we transplanted adult females from a solitary, northern population, to a southern site where native bees are typically eusocial. Nearly all native nests were eusocial, with foundresses producing small first brood (B1) females that became workers. In contrast, nine out of ten nests initiated by transplanted bees were solitary, producing female offspring that were the same size as the foundress and entered directly into hibernation. Only one of these ten nests became eusocial. Social phenotype was unlikely to be related to temperature experienced by nest foundresses when provisioning B1 offspring, or by B1 emergence time, both previously implicated in social plasticity seen in two other socially polymorphic sweat bees. Our results suggest that social polymorphism in L. calceatum predominantly reflects genetic differentiation between populations, and that plasticity is in the process of being lost by bees in northern populations. Phenotypic plasticity is thought to play a key role in the early stages of the transition from solitary to eusocial behaviour, but may then be lost if environmental conditions become less variable. Socially polymorphic sweat bees exhibit either solitary or eusocial behaviour in different geographic populations, depending on the length of the nesting season. We tested for plasticity in the socially polymorphic sweat bee Lasioglossum calceatum by transplanting nest foundresses from a northern, non-eusocial population to a southern, eusocial population. Plasticity would be detected if transplanted bees exhibited eusocial behaviour. We found that while native bees were eusocial, 90% of transplanted bees and their offspring did not exhibit traits associated with eusociality. Environmental variables such as time of offspring emergence or temperatures experienced by foundresses during provisioning could not explain these differences. Our results suggest that the ability of transplanted bees to express eusociality is being lost, and that social polymorphism predominantly reflects genetic differences between populations.

Relatedness is predicted to be a key determinant of cooperative behavior, but kin discrimination within social insect colonies is surprisingly rare. A lack of reliable cuticular hydrocarbon (CHC) cues is thought to be responsible, but here we show that in a high-profile paper wasp model, kin recognition cues are available for some individuals that found nests with nonrelatives. Thus, unrelated Polistes dominulus helpers could potentially recognize themselves as such. On this basis, we reanalyzed a behavioral data set to investigate whether foraging effort, defense contributions and aggression toward nest mates might thus reflect CHC profiles. Both foraging behavior and aggression varied with genetic relatedness, but genetic relatedness itself was a better predictor of this variation than differences in CHC profiles. We propose that wasps use specific components of the CHC profile, the identity of which is as yet unknown, to identify relatives among nest mates. Our data provide the first evidence of within-nest kin discrimination in primitively eusocial wasps but leave open the question of which cues are responsible.

Eusocial animal societies are typified by the presence of a helper (worker) caste which predominantly cares for young offspring in a social group while investing little in their own direct reproduction. A key question is what determines whether an individual becomes a worker or leaves to initiate her own reproduction. In some insects, caste is determined nutritionally during development. In others, and in vertebrate societies, adults are totipotent and the cues that determine caste are less well known. The mate limitation hypothesis (MLH) states that a female's mating status acts as a cue for caste determination: females that mate become reproductives, while those that fail to mate become workers. The MLH is consistent with empirical observations in sweat bees showing that over the course of the nesting season, there are increases in both the proportion of females that become reproductives and the frequency of males in the mating pool. We modelled a foundress's offspring sex-ratio strategy to investigate whether an increasingly male-biased operational sex-ratio over time is evolutionarily stable under the MLH. Our results indicate that such a pattern could occur if early workers were more valuable than late workers. This pattern was then more likely if male mortality was high, if worker mortality was low, if the value of a worker was high and if the period over which workers can help was short. Our results suggest that the MLH can be evolutionarily stable, but only under restrictive conditions. Manipulative experiments are now required to investigate whether mating determines caste in nature.

In cooperatively breeding vertebrates, the existence of individuals that help to raise the offspring of non-relatives is well established, but unrelated helpers are less well known in the social insects. Eusocial insect groups overwhelmingly consist of close relatives, so populations where unrelated helpers are common are intriguing. Here, we focus on Polistes dominula— the best-studied primitively eusocial wasp, and a species in which nesting with non-relatives is not only present but frequent. We address two major questions: why individuals should choose to nest with non-relatives, and why such individuals participate in the costly rearing of unrelated offspring. Polistes dominula foundresses produce more offspring of their own as subordinates than when they nest independently, providing a potential explanation for co-founding by non-relatives. There is some evidence that unrelated subordinates tailor their behaviour towards direct fitness, while the role of recognition errors in generating unrelated co-foundresses is less clear. Remarkably, the remote but potentially highly rewarding chance of inheriting the dominant position appears to strongly influence behaviour, suggesting that primitively eusocial insects may have much more in common with their social vertebrate counterparts than has commonly been thought.

Our knowledge of primitively eusocial societies is focused particularly on cooperatively breeding vertebrates and vespid wasps, whereas numerous taxa representing independent origins of social behavior have been largely overlooked. The lineage of apoid wasps including the genus Microstigmus represents a relatively neglected independent origin of eusociality. We present the first use of modern hypervariable genetic markers, in combination with behavioral observations, to investigate reproductive division of labor and cooperative brood care in an apoid wasp, the Brazilian M. nigrophthalmus. Microstigmus nigrophthalmus is unusual because, although there is cooperative brood care, reproductively dominant females carry out at least as much risky foraging as their subordinate nest mates. Empirical studies of reproductive skew are often hampered by a lack of variation in skew. We find that reproductive skew is highly variable between nests in M. nigrophthalmus. There was no correlation between skew and either body size or group size. The absence of an effect of body size is typical of studies of skew in insects and may indicate that body size is a poor measure of an individual's ability to control a group. However, skew was positively correlated with genetic relatedness. This provides rare support for concession models based on "social contracts" between dominant individuals and their subordinates. Copyright 2011, Oxford University Press.

The origin of eusociality is often regarded as a change of macroevolutionary proportions [[1] and [2]]. Its hallmark is a reproductive division of labor between the members of a society: some individuals (?helpers? or ?workers?) forfeit their own reproduction to rear offspring of others (?queens?). In the Hymenoptera (ants, bees, wasps), there have been many transitions in both directions between solitary nesting and sociality [[2], [3], [4] and [5]]. How have such transitions occurred? One possibility is that multiple transitions represent repeated evolutionary gains and losses of the traits underpinning sociality. A second possibility, however, is that once sociality has evolved, subsequent transitions represent selection at just one or a small number of loci controlling developmental switches between preexisting alternative phenotypes [[2] and [6]]. We might then expect transitional populations that can express either sociality or solitary nesting, depending on environmental conditions. Here, we use field transplants to directly induce transitions in British and Irish populations of the sweat bee Halictus rubicundus. Individual variation in social phenotype was linked to time available for offspring production, and to the genetic benefits of sociality, suggesting that helping was not simply misplaced parental care [7]. We thereby demonstrate that sociality itself can be truly plastic in a hymenopteran.

Environmental factors, and particularly climate, play an important role in influencing behaviour in many insects. In social species, climate is known to have a strong influence on social traits, but how this manifests itself in tropical ecosystems is poorly understood. In Peninsular Malaysia, the climate is characterised by relatively consistent annual temperatures with wet/dry cycles, and the tropical hover-wasp Liostenogaster flavolineata Cameron is active year-round. Newly emerged females can choose to remain at the natal nest and help, or disperse and found their own nest depending on a balance of ecological and demographic factors. We collated long-term adult and brood census data for populations of L. flavolineata in Peninsular Malaysia in three different years to investigate temporal variation in demographics (brood and adult numbers) and how this might be related to climatic factors. Our data indicate that there are multiple, temporally distinct peaks of brood production in this population. The number of newly eclosing females and number of mature brood were positively associated with temperature and negatively associated with the number of rain-days during the observation period. Furthermore, larger females were produced during the peaks of brood production. We speculate how these patterns may influence the staying or leaving decisions of newly emerged females in a primitively eusocial species such as L. flavolineata.

In primitively eusocial societies, all individuals can potentially reproduce independently. The key fact that we focus on in this paper is that individuals in such societies instead often queue to inherit breeding positions. Queuing leads to systematic differences in expected future fitness. We first discuss the implications this has for variation in behaviour. For example, because helpers nearer to the front of the queue have more to lose, they should work less hard to rear the dominant's offspring. However, higher rankers may be more aggressive than low rankers, even if they risk injury in the process, if aggression functions to maintain or enhance queue position. Second, we discuss how queuing rules may be enforced through hidden threats that rarely have to be carried out. In fishes, rule breakers face the threat of eviction from the group. In contrast, subordinate paper wasps are not injured or evicted during escalated challenges against the dominant, perhaps because they are more valuable to the dominant. We discuss evidence that paper-wasp dominants avoid escalated conflicts by ceding reproduction to subordinates. Queuing rules appear usually to be enforced by individuals adjacent in the queue rather than by dominants. Further manipulative studies are required to reveal mechanisms underlying queue stability and to elucidate what determines queue position in the first place.

The sweat bees (Family Halictidae) are a socially diverse taxon in which eusociality has arisen independently numerous times. The obligate, primitively eusocial Lasioglossum malachurum, distributed widely throughout Europe, has been considered the zenith of sociality within halictids. A single queen heads a colony of smaller daughter workers which, by mid-summer, produce new sexuals (males and gynes), of which only the mated gynes overwinter to found new colonies the following spring. We excavated successfully 18 nests during the worker- and gyne-producing phases of the colony cycle and analysed each nest's queen and either all workers or all gynes using highly variable microsatellite loci developed specifically for this species. Three important points arise from our analyses. First, queens are facultatively polyandrous (queen effective mating frequency: range 1?3, harmonic mean 1.13). Second, queens may head colonies containing unrelated individuals (n= 6 of 18 nests), most probably a consequence of colony usurpation during the early phase of the colony cycle before worker emergence. Third, nonqueen's workers may, but the queen's own workers do not, lay fertilized eggs in the presence of the queen that successfully develop into gynes, in agreement with so-called `concession? models of reproductive skew.

The mechanisms through which dominance is inherited within social groups vary from direct interactions such as fighting to non-confrontational conventions. Liostenogaster flavolineata is a primitively eusocial hover wasp in which one female, the ‘dominant’, is the only reproductive upon the nest. The remaining females, although capable of reproduction, behave as helpers. In this study, we investigate the rules by which helpers inherit dominance. We removed successive dominants from 56 nests and recorded accession on un-manipulated nests. The results showed that L. flavolineata has a strict age-based inheritance queue: new dominants are the oldest female in their groups 87% of the time. Thirteen cases of queue-jumping were found in which young individuals were able to supplant older nestmates and inherit dominance precociously. Queue jumpers did not differ from other wasps in terms of relatedness to other group members or body size. Individuals that had previously worked less hard than other females of equivalent rank were significantly more likely to later jump the queue. Queue-jumping may represent a cheating strategy or could indicate that the rule for inheriting dominance is not based purely on relative age. We also discuss possible reasons why age-based queuing has evolved and its potential to promote the evolution of helping behaviour.

An important benefit of social living is increased capacity for defense. Highly eusocial species have often evolved a fighting caste for this purpose, but many facultatively eusocial insects and cooperatively breeding vertebrates lack morphological castes and the decision to defend or not can depend on costs and benefits to each individual. Defense by subordinates in a social group can be regarded as a form of helping, and helping input often varies among subordinates of different age or size. Several hypotheses attempt to explain variation in helping effort, including the effects of relatedness and differences in the costs of helping. Evidence for these hypotheses is mixed and often lacks data on the rank of subordinates, an important determinant of expected future fitness. We examined individual variation in propensity to defend the nest against conspecifics in the tropical hairy-faced hover wasp Liostenogaster flavolineata. Prior to experimentation, we determined the positions of all wasps in the age-based queue to inherit the single egg-laying position in each L. flavolineata group. Two approaches were then used: observations of defense against natural intrusions by conspecifics and experimental trials where wasps were presented attached to a wire. Higher ranks were more likely to defend the nest than lower ranks, opposite to the pattern previously documented for another form of helping: foraging effort. Possible explanations for this result are that higher ranked females are better defenders and that they suffer a larger decrease in expected future fitness when an intruder usurps their position in the inheritance queue. Copyright 2007, Oxford University Press.

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

Helpers in primitively eusocial and cooperatively breeding animal societies forfeit their own reproduction to rear the offspring of a queen or breeding pair, but may eventually attain breeding status themselves. Kin selection1 provides a widely accepted theoretical framework for understanding these societies, but differences in genetic relatedness do not explain a universal societal feature: the huge variation between individuals in helping effort2,3,4,5,6,7,8,9,10. An alternative explanation for this variation lies in a fundamental trade-off faced by helpers: by working harder, they increase the indirect component of their fitness, but simultaneously decrease their own future survival and fecundity2,4,8. Here, we show that individuals work less hard when they stand to lose more future fitness through working. We experimentally manipulated two components of future fitness in social queues of hover wasps (Stenogastrinae): a helper's chance of inheriting an egg-laying position, and the workforce available to rear her offspring should she inherit. After each manipulation, helpers increased or decreased their effort as appropriate to the change in expected future fitness that they experienced. Although helping provides significant indirect fitness benefits for hover wasps11, our study shows that variation in the costs associated with helping is the major determinant of helping effort.

The degree of genetic heterogeneity among the individuals in an animal society depends on the society's genetic structure. Genetic heterogeneity, in turn, means that group members will differ in their reproductive objectives and conflicts over reproduction may arise. The resolution of these conflicts may be reflected in the way that reproduction is partitioned between potential reproductives. We used 5 microsatellite loci to investigate genetic structure and reproductive skew in 17 nests of the Malaysian hover wasp, Parischnogaster alternata. Parischnogaster alternata colonies are small (1--10 females), and all adult colony members are capable of mating and producing offspring. We found that colonies tended to consist of closely related individuals and that at any one time the production of both female and male offspring was nearly always monopolized by a single dominant female, despite considerable variation between nests in parameters predicted to affect skew. Subordinate females that remained in their natal colonies obtained indirect fitness benefits by helping to raise offspring to which they were related. Subordinate females also appeared to be positioned within an age-based queue for inheritance of the dominant egg-laying position. We suggest that the high skew in P. alternata may result from strong ecological constraints on solitary nesting, high relatedness, and a relatively high probability that subordinates will eventually inherit the position of dominance. Copyright 2006.

Most nonsocial wasps and bees are mass provisioners (MP), sealing each egg into its own cell containing all of the food required to reach maturity. Other species instead provision progressively, feeding their offspring only gradually as they develop and usually provisioning more than one offspring simultaneously (SPP). The evolution of progressive provisioning is interesting because it has obvious drawbacks. In particular, it could prolong the period of offspring dependency, and hence increase the chance that a mother will die before her offspring reach independence. Prolonged dependency could in turn facilitate the evolution of helping through insurance-based mechanisms. In this paper, I outline two ecologically extreme models of how reproductive success is accrued during provisioning. In Model 1, immature offspring become independent as soon as they are fully provisioned. SPP is then disadvantageous because it prolongs the provisioning period compared with MP. If SPP does evolve, Model 1 predicts that brood size, the number of offspring provisioned simultaneously in a batch, should be minimized. Model 2 differs from Model 1 in that offspring become independent only at adulthood. SPP can then be advantageous because investment is converted into independent offspring more quickly than under MP. Model 2 predicts an intermediate brood size, positively correlated with larval development time and the abundance of provisions. Ammophiline digger wasps and eusocial vespids may correspond to Models 1 and 2, respectively, whereas ground-nesting wasps and bees with multicellular nests may be intermediate. Copyright 2005.

We explore the effects of group size on the direct reproductive success of subordinate helpers in eusocial animals where only a single, dominant individual reproduces at one time. Helpers can reproduce directly if they inherit dominance, but when dominance is age based, an individual born into a larger group has a longer wait to inherit. We show that this disincentive to help can potentially be offset by increased productivity, increased life span, and insurance-based benefits for helpers if they survive to inherit dominance in larger groups. We analyze a field experiment in which group size was manipulated in the hover wasp Liostenogaster flavolineata. Productivity increased linearly with group size, larger groups were less likely to fail, and dominants in larger groups may have lived longer. Combined with the probability of inheriting dominance, these effects led overall to a negative correlation between group size and expected direct fitness, mainly because group size decreased during our study period, so that helpers could not expect to inherit as large a group as they started queuing in. Our analysis suggests that the relationship between group size and productivity plays a central role in determining the fitness consequences of helping.

In facultatively eusocial hover wasps, some females leave their natal nests while others choose to stay and become helpers. We tested whether the decisions of 126 newly emerged females to stay or leave depended on group size: the number of females already resident on their natal nests. We predicted that females would be less likely to stay in larger groups, where the benefits of helping are probably smaller and there is a smaller chance of inheriting the dominant position. We also predicted that unrelated females would be less likely to join larger groups. We manipulated group size by removing residents from nests. Newly emerged females disappeared from their natal nests at a rate of 2.5% per day, but did not disappear from manipulated nests at higher rates than controls. Experimentally reducing group size also did not increase the frequency of joiners. Newly emerged females disappeared at twice the rate of older subordinate females, suggesting the existence of a `leaving window' early in life. One problem is the difficulty of distinguishing between leaving and death.

The evolution of helping, in which some individuals forfeit their own reproduction and help others to reproduce, is a central problem in evolutionary biology. Recently proposed insurance-based mechanisms rely on a pre-existing life history with a long period of offspring dependency relative to the short life expectancies of adult carers1, 2, 3, 4: a lone mother's offspring are doomed if she dies young, whereas after a helper dies, other group members can finish rearing the offspring5, 6. A critical question, however, is how this life history could evolve in ancestral non-social populations, as offspring survival would then depend on a single, short-lived carer. Here, we resolve this paradox by focusing on the extended parental care inherent in prolonged dependency. We show experimentally that in non-social wasps, extended care can significantly reduce the impact of interspecific parasites. Under extended care, offspring are less vulnerable by the time they are exposed to parasites, and costs of parasitism are reduced because mothers have the option to terminate investment in failing offspring. By experimentally simulating aspects of extended care in a species where it is lacking, we demonstrate that neither benefit requires specialized behaviour. Such benefits could therefore offset the disadvantage of prolonged dependency in non-social species, thereby facilitating the evolution of helping.

Sweat bees (family Halictidae) comprise a numerous and diverse group that are arguably among the most socially labile of all insect taxa. Given the lack of highly variable markers for eusocial species of the family, we developed a suite of dinucleotide and trinucleotide markers for one of its members, the Eurasian Lasioglossum malachurum, and used them to amplify DNA from other halictids. Loci were highly variable in L. malachurum and amplified DNA from many other halictids.

Climate has long been suggested to affect population genetic structures of eusocial insect societies. For instance, Hamilton [Journal of Theoretical Biology 7 (1964) 17] discusses whether temperate and tropical eusocial insects may show differences in population-level genetic structure and viscosity, and how this might relate to differences in the degree of synchrony in their life cycles or modes of nest founding. Despite the importance of Hamilton's 1964 papers, this specific idea has not been tested in actual populations of wasps, probably due to the paucity of studies on tropical species. Here, we compare colony and population genetic structures in two species of primitively eusocial paper wasps with contrasting ecologies: the tropical species Polistes canadensis and the temperate species P. dominulus. Our results provide important clarifications of Hamilton's discussion. Specifically, we show that the genetic structures of the temperate and tropical species were very similar, indicating that seasonality does not greatly affect population viscosity or inbreeding. For both species, the high genetic differentiation between nests suggests strong selection at the nest level to live with relatives, whereas low population viscosity and low genetic differentiation between nest aggregations might reflect balancing selection to disperse, avoiding competition with relatives. Overall, our study suggests no prevalence of seasonal constraints of the life cycle in affecting the population genetic structure of eusocial paper wasps. These conclusions are likely to apply also to other primitively eusocial insects, such as halictine bees. They also highlight how selection for a kin structure that promotes altruism can override potential effects of ecology in eusocial insects. © 2012 The Authors.Ecology and Evolution published by Blackwell Publishing Ltd.

Animals that cooperate with nonrelatives represent a challenge to inclusive fitness theory, unless cooperative behavior is shown to provide direct fitness benefits. Inheritance of breeding resources could provide such benefits, but this route to cooperation has been little investigated in the social insects. We show that nest inheritance can explain the presence of unrelated helpers in a classic social insect model, the primitively eusocial wasp Polistes dominulus. We found that subordinate helpers produced more direct offspring than lone breeders, some while still subordinate but most after inheriting the dominant position. Thus, while indirect fitness obtained through helping relatives has been the dominant paradigm for understanding eusociality in insects, direct fitness is vital to explain cooperation in P. dominulus.

International audience; Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

The paper wasp Polistes dominulus is unique among the social insects in that nearly one-third of co-foundresses are completely unrelated to the dominant individual whose offspring they help to rear and yet reproductive skew is high. These unrelated subordinates stand to gain direct fitness through nest inheritance, raising the question of whether their behaviour is adaptively tailored towards maximizing inheritance prospects. Unusually, in this species, a wealth of theory and empirical data allows us to predict how unrelated subordinates should behave. Based on these predictions, here we compare helping in subordinates that are unrelated or related to the dominant wasp across an extensive range of field-based behavioural contexts. We find no differences in foraging effort, defense behaviour, aggression or inheritance rank between unrelated helpers and their related counterparts. Our study provides no evidence, across a number of behavioural scenarios, that the behaviour of unrelated subordinates is adaptively modified to promote direct fitness interests.\ud \ud

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

The origin and maintenance of eusociality is a central problem in evolutionary biology1, 2. Eusocial groups contain individuals that forfeit their own reproduction in order to help others reproduce. In facultatively eusocial taxa, offspring can choose whether to found new nests or become helpers in their natal groups. In many facultatively eusocial insects, offspring need continuous care during development, but adult carers have life expectancies shorter than the developmental period3, 4, 5, 6, 7. When a lone foundress dies, her partly reared brood are usually doomed. Here, we show that helpers in a tropical hover wasp (Liostenogaster flavolineata) have an insurance-based advantage over lone foundresses because after a helper dies, most of the brood that she has partly reared will be brought to maturity by surviving nest-mates. After some of the helpers are experimentally removed from a multi-female nest, the reduced group is left with more brood than it would normally rear. We found that larger, more valuable extra brood were reared through to maturity, but not smaller, less valuable brood. Smaller brood may be sacrificed to feed larger brood, and reduced groups probably benefited from increased short-term helper recruitment. Rearing extra brood did not increase adult mortality or brood development time.

A candidate explanation for the evolution of eusociality is that helpers are physiologically constrained such that helping is their only realistic option. We tested this subfertility hypothesis in a species of facultatively eusocial hover wasp (Hymenoptera, Stenogastrinae: Liostenogaster flavolineata) by seeing whether helpers that were forced to nest on their own were able to mature their own eggs. One focal helper was left alone on each of 22 nests, from which all other adult wasps (including the dominant) were permanently removed. After 18 days, all but one of the 19 focal helpers that remained on their nests had ovarian development and insemination status characteristic of dominants, and the majority had probably laid eggs. This was in striking contrast to the reproductive status of other helpers removed from the same nests at the start of the experiment. These results provide convincing experimental evidence that females do not become helpers because of some unconditional physiological constraint. There is currently no unequivocal support for the subfertility hypothesis in facultatively eusocial Hymenoptera lacking morphological castes. Copyright 1999 The Association for the Study of Animal Behaviour.

Recent field experiments suggest that cooperative breeding in vertebrates can be driven by a shortage of breeding territories. We did analogous experiments on facultatively eusocial hover wasps (Stenogastrinae: Liostenogaster flavolineata). We provided nesting opportunities by removing residents from 39 nests within a large aggregation (1995), and by glueing 20 nests obtained from a distant site into a second aggregation (1996). We prevented nest-less floaters from competing for these opportunities in 1995 but not in 1996. In both years, helpers in unmanipulated groups were given opportunities to nest independently without having to incur nest-building costs and with a reduced wait before potential helpers emerged. Helpers visited the nests we provided, but adopted only a small proportion (5% of 111 vacancies created in 1995). Others were adopted by floaters, but a significant proportion of nests were never adopted (nine out of 20 in 1995, seven out of 20 in 1996). Helpers that visited nests did not originate from particular kinds of social group. Nests containing older brood were more likely to be adopted, and adopting females rarely destroyed older brood. A general feature of social insect but not vertebrate life-histories, the long period of offspring dependency relative to the short life expectancy of adult carers, may be a key factor constraining independent nesting.

Temperate-zone socially polymorphic sweat bees (Hymenoptera: Halictidae) are ideal model systems for elucidating the origins of eusociality, a major evolutionary transition. Bees express either social or solitary behaviour in different parts of their range, and social phenotype typically correlates with season length. Despite their obvious utility, however, socially polymorphic sweat bees have received relatively little attention with respect to understanding the origins of eusociality. Lasioglossum (Evylaeus) calceatum is a widespread sweat bee that is thought to be socially polymorphic, with important potential as an experimental model species. We first determined the social phenotype of L. calceatum at three sites located at different latitudes within the UK. We then investigated sociality in detail across two years at the southernmost site. We found that L. calceatum exhibits latitudinal social polymorphism within the UK; bees were solitary at our two northern sites but the majority of nests were social at our southern site. Sociality in the south was characterised by a relatively small mean of two and 3.5 workers per nest in each year, respectively, and a small to medium mean caste-size dimorphism of 6.6 %. Foundresses were smaller in our more northern and high altitude populations. Sociality is clearly less specialised than in some closely related obligately social species but probably more specialied than other polymorphic sweat bees. Our research provides a starting point for future experimental work to investigate mechanisms underlying social polymorphism in L. calceatum.

Maternal effects should be especially likely when mothers actively provision offspring with resources that influence offspring phenotype. In cooperatively breeding and eusocial taxa, there is potential for parents to strategically manipulate offspring phenotype in their own interests. Social insect queens are nearly always larger than their worker offspring, and queens could benefit by producing small daughter workers in several ways. If queens use aggression to dominate or coerce workers, a queen producing small workers might minimize potential conflict or competition from her offspring. In addition, because of the trade-off between the number of workers she is able to produce and their individual size, a queen may produce small workers to optimize colony work effort. In this study, we investigate why queens of the primitively eusocial paper wasp Polistes gallicus limit the size of their workers. We created queen–worker size mismatches by cross-fostering queens between nests. We then tested whether the queen–worker size difference affects worker foraging and reproductive effort, or the amount of aggression in the group. Some of our results were consistent with the idea that queens limit worker size strategically: small workers were no less successful foragers, so that producing a larger number of smaller workers may overall increase queen fitness. We found that queens were less likely to attack large workers, perhaps because attempting to coerce large workers is riskier. However, larger workers did not forage less, did not invest more in ovarian development, and were not more aggressive themselves. There was therefore little evidence overall that queens limit conflict by producing smaller workers. Significance statement In social animals, parents might manipulate phenotypic traits of their offspring in their own interests. In paper wasps (Polistes), the first offspring produced are smaller than the queen and become workers: instead of founding their own nests, they stay and help their mother to rear new queens and males. We investigated whether P. gallicus queens could benefit by producing small daughter workers by using cross-fostering to create size mismatches between queens and their offspring. We then recorded foraging activity, reproductive effort, and aggression on nests. Queens were less likely to attack larger workers, but overall, there was limited evidence of size-based queen–worker conflict. However, because small workers were no less successful foragers, producing a larger number of smaller workers may optimize colony work effort.