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Abstract Plasticity is a key trait when an individual’s role in the social environment, and hence its optimum phenotype, fluctuates unpredictably. Plasticity is especially important in primitively eusocial insects where small colony sizes and little morphological caste differentiation mean that individuals may find themselves switching from non-reproductive to reproductive roles. To understand the scope of this plasticity, workers of the primitively eusocial sweat bee Lasioglossum malachurum were experimentally promoted to the reproductive role (worker-queens) and their performance compared with foundress-queens. We focussed on how their developmental trajectory as workers influenced three key traits: group productivity, monopolisation of reproduction, and social control of foraging nest-mates. No significant difference was found between the number of offspring produced by worker-queens and foundress-queens. Genotyping of larvae showed that worker-queens monopolised reproduction in their nests to the same extent as foundress queens. However, non-reproductives foraged less and produced a smaller total offspring biomass when the reproductive was a promoted worker: offspring of worker-queens were all males, which are the cheaper sex to produce. Greater investment in each offspring as the number of foragers increased suggests a limit to both worker-queen and foundress-queen offspring production when a greater quantity of pollen arrives at the nest. The data presented here suggest a remarkable level of plasticity and represent one of the first quantitative studies of worker reproductive plasticity in a non-model primitively eusocial species. Significance statement The ability of workers to take on a reproductive role and produce offspring is expected to relate strongly to the size of their colony. Workers in species with smaller colony sizes should have greater reproductive potential to insure against the death of the queen. We quantified the reproductive plasticity of workers in small colonies of sweat bees by removing the queen and allowing the workers to control the reproductive output of the nest. A single worker then took on the reproductive role and hence prevented her fellow workers from producing offspring of their own. These worker-queens produced as many offspring as control queens, demonstrating remarkable worker plasticity in a primitively eusocial species.

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.

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.

Phenotypic plasticity may evolve when conditions vary temporally or spatially on a small enough scale. Plasticity is thought to play a central role in the early stages of evolutionary transitions, including major transitions such as those between non-sociality and sociality. The sweat bee Halictus rubicundus is of special interest in this respect, because it is socially plastic in the British Isles: Nests are social or non-social depending on the environment. However, sociality comprises a complex suite of inter-related traits. To further investigate social plasticity in H. rubicundus, we measured traits that are potentially integral to social phenotype at a northern site, where nests are non-social, and a southern site where nests can be social. We found that foundresses at non-social sites were smaller, produced offspring of a size more similar to themselves, initiated nesting later, and took longer to produce their first female offspring. They began provisioning earlier in the day, finished earlier, and collected more pollen loads. Common garden experiments suggested that these differences represent mainly plasticity, as expected for traits involved in the overall plastic social phenotype, with only limited evidence for fixed genetic differences in foraging. Conditions during overwintering did not have major effects on a foundress' subsequent behaviour.

Altruism in the social Hymenoptera is generally considered to be a feature of females rather than males. A popular explanation for this is that in the solitary ancestors of today's social species, males provided little brood care. Males might therefore lack the preadaptations necessary to evolve altruism in social contexts. While anecdotal observations of male contributions to colony life have been reported, there are few reports of male participation in nest defence. In apoid wasps, there have been several reports of male nest-guarding behaviour in solitary species, potentially setting the evolutionary stage for similar behaviours in social lineages. Here, we present evidence of active and effective nest defence in males of the social apoid wasp Microstigmus nigrophthalmus. Males were observed chasing intruders away from the nest, and the presence of males had a significant effect on nest survival when females were removed. Males potentially obtained direct benefits through defence, so that defence may not represent male altruism. However, our results do show that males can perform acts that benefit their colony.

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.

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 progression from solitary living to caste-based sociality is commonly regarded as a major evolutionary transition. However, it has recently been shown that in some taxa, sociality may be plastic and dependent on local conditions. If sociality can be environmentally driven, the question arises as to how projected climate change will influence features of social organisation that were previously thought to be of macroevolutionary proportions. Depending on the time available in spring during which a foundress can produce worker offspring, the sweat bee Halictus rubicundus is either social or solitary. We analysed detailed foraging data in relation to climate change predictions for Great Britain to assess when and where switches from a solitary to social lifestyle may be expected. We demonstrate that worker numbers should increase throughout Great Britain under predicted climate change scenarios, and importantly, that sociality should appear in northern areas where it has never before been observed. This dramatic shift in social organisation due to climate change should lead to a bigger workforce being available for summer pollination and may contribute towards mitigating the current pollinator crisis. Significance Statement The sweat bee Halictus rubicundus is socially polymorphic, expressing both solitary and social forms, and is socially plastic, capable of transitioning from solitary to social forms, depending on local environmental conditions. Here, we analyse detailed foraging data in relation to climate change predictions for Great Britain to show that worker numbers and sociality both increase under predicted climate change scenarios. Especially dramatic will be the appearance of social H. rubicundus nests in the north of Britain, where previously only solitary forms are found. Particularly, if more taxa are found to be socially plastic, environmentally driven shifts in social organisation may help to mitigate future pollinator crises by providing more individuals for pollination. Electronic supplementary material The online version of this article (doi:10.1007/s00265-016-2118-y) contains supplementary material, which is available to authorized users.

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.