Worker biting interactions and task performance in a swarm-founding eusocial wasp (Polybia occidentalis, Hymenoptera: Vespidae)

Workers in many insect societies interact via body contact withtheir nest mates, and social biting and other forms of contactmay play a general role in regulating task performance. HereI present evidence that social biting affects task performancewithout direct reproductive conflict in Polybia occidentalis,a swarm-founding eusocial wasp. Polybia occidentalis workersengaged in social biting with nest mates. Most workers thatwere active on the nest surface participated in biting interactions,but individuals differed significantly in their rates of biting and of being bitten. Rates of being bitten corresponded withnonreproductive task performance: more biting was directedat foragers than nonforagers, and foraging rates were correlatedwith rates of being bitten. Furthermore, some on-nest workersinitiated foraging activity immediately after they were bitten.Together these patterns suggest that social biting influencesforaging rates by increasing workers' probabilities of leavingthe nest. Variation in biting rates did not correspond withdifferences in reproductive physiology: highly active bitersand recipients did not differ in body size or in ovary development.In P. occidentalis and in other eusocial insects with largeworker forces, biting and other types of social contact amongworkers may regulate task performance independently of directreproductive competition.     

Division of labour and seasonality in the ant Leptothorax albipennis: worker corpulence and its influence on behaviour

We address the organization of workers in social insect societies. We distinguish between changes in behavioural role over the nurse to forager role sequence, which may depend on changes in physiology, and potentially more rapid changes of task within role. We investigated the association between role and nutrient status in the ant Leptothorax albipennis. Worker lipid stores were quantified using a new body size-controlled method, and were related to worker behaviour. Worker lipid stores were evenly distributed amongst colony members at the end of winter, splitting rapidly into two distinct modes (replete nurses and lean foragers) in spring. The proportion of lean foragers increased throughout spring and summer, until most colonies contained only workers of this type. Callow workers then eclosed with intermediate lipid stores. We developed a computer vision system that tracks all nest ants to extract detailed behaviour of individuals of known lipid stores. Lipid storage was negatively correlated with a worker's foraging propensity, and with measures of spatial occupation in the nest and of activity. Different colonies showed a similar quantitative correlation between lipid stores and behavioural role, suggesting that lipid stores were not only correlated with the relative organization of individuals within each nest, but may also have influenced their absolute role. We reviewed the literature and found evidence that nutrient status influences role predisposition in social insect workers. We conclude that the distribution of worker roles may be linked to the balance between foraging income and energetic consumption within the colony directly via worker nutrient status. Copyright 2000 The Association for the Study of Animal Behaviour.     

Task-specific expression of the foraging gene in harvester ants

In social insects, groups of workers perform various tasks such as brood care and foraging. Transitions in workers from one task to another are important in the organization and ecological success of colonies. Regulation of genetic pathways can lead to plasticity in social insect task behaviour. The colony organization of advanced eusocial insects evolved independently in ants, bees, and wasps and it is not known whether the genetic mechanisms that influence behavioural plasticity are conserved across species. Here we show that a gene associated with foraging behaviour is conserved across social insect species, but the expression patterns of this gene are not. We cloned the red harvester ant (Pogonomyrmex barbatus) ortholog (Pbfor) to foraging, one of few genes implicated in social organization, and found that foraging behaviour in harvester ants is associated with the expression of this gene; young (callow) worker brains have significantly higher levels of Pbfor mRNA than foragers. Levels of Pbfor mRNA in other worker task groups vary among harvester ant colonies. However, foragers always have the lowest expression levels compared to other task groups. The association between foraging behaviour and the foraging gene is conserved across social insects but ants and bees have an inverse relationship between foraging expression and behaviour.     

Evolution of the neuronal substrate for kin recognition in social Hymenoptera

In evolutionary terms, life is about reproduction. Yet, in some species, individuals forgo their own reproduction to support the reproductive efforts of others. Social insect colonies for example, can contain up to a million workers that actively cooperate in tasks such as foraging, brood care and nest defence, but do not produce offspring. In such societies the division of labour is pronounced, and reproduction is restricted to just one or a few individuals, most notably the queen(s). This extreme eusocial organisation exists in only a few mammals, crustaceans and insects, but strikingly, it evolved independently up to nine times in the order Hymenoptera (including ants, bees and wasps). Transitions from a solitary lifestyle to an organised society can occur through natural selection when helpers obtain a fitness benefit from cooperating with kin, owing to the indirect transmission of genes through siblings. However, this process, called kin selection, is vulnerable to parasitism and opportunistic behaviours from unrelated individuals. An ability to distinguish kin from non-kin, and to respond accordingly, could therefore critically facilitate the evolution of eusociality and the maintenance of non-reproductive workers. The question of how the hymenopteran brain has adapted to support this function is therefore a fundamental issue in evolutionary neuroethology. Early neuroanatomical investigations proposed that social Hymenoptera have expanded integrative brain areas due to selection for increased cognitive capabilities in the context of processing social information. Later studies challenged this assumption and instead pointed to an intimate link between higher social organisation and the existence of developed sensory structures involved in recognition and communication. In particular, chemical signalling of social identity, known to be mediated through cuticular hydrocarbons (CHCs), may have evolved hand in hand with a specialised chemosensory system in Hymenoptera. Here, we compile the current knowledge on this recognition system, from emitted identity signals, to the molecular and neuronal basis of chemical detection, with particular emphasis on its evolutionary history. Finally, we ask whether the evolution of social behaviour in Hymenoptera could have driven the expansion of their complex olfactory system, or whether the early origin and conservation of an olfactory subsystem dedicated to social recognition could explain the abundance of eusocial species in this insect order. Answering this question will require further comparative studies to provide a comprehensive view on lineage-specific adaptations in the olfactory pathway of Hymenoptera.     

Reproductive physiology, dominance interactions, and division of labour among bumble bee workers

Abstract. Bumble bee workers (Bombus bifarius, Hymenoptera: Apidae) exhibit aggression toward one another after the colony begins producing female reproductive offspring (the competition phase). Workers in competition phase colonies must continue to perform in‐nest tasks, such as nest thermoregulation, and to forage for food, to rear the reproductives to maturity. Therefore, competition phase workers are faced with potentially conflicting pressures to work for their colonies, or to compete for direct reproduction. The effects of reproductive competition on worker task performance were quantified by measuring relationships of worker body size, reproductive physiology, and aggression with their rates of task performance. If worker division of labour was strongly affected by competition, it was predicted that fecund workers would avoid performing nest maintenance and foraging tasks, focusing instead on reproductive behaviour. Furthermore, it was predicted that fecund workers would dominate their nest mates, and that subordinate workers would perform nonreproductive tasks at higher rates. Worker aggression was associated closely with direct reproductive competition. Both aggression and brood interaction rates were related positively with ooctye development. Furthermore, foraging was associated negatively with ovarian development. However, in‐nest and foraging task performance rates were not associated with social aggression. The results support a partial role for reproductive competition in worker polyethism. Although worker aggression did not directly affect polyethism, reproductively competent workers avoided foraging tasks that would remove them from egg‐laying opportunities. Reproductively competent workers did perform in‐nest tasks, suggesting that these tasks entail little cost in terms of reproductive competition.     

Physiological variation as a mechanism for developmental caste-biasing in a facultatively eusocial sweat bee

Social castes of eusocial insects may have arisen through an evolutionary modification of an ancestral reproductive ground plan, such that some adults emerge from development physiologically primed to specialize on reproduction (queens) and others on maternal care expressed as allo-maternal behaviour (workers). This hypothesis predicts that variation in reproductive physiology should emerge from ontogeny and underlie division of labour. To test these predictions, we identified physiological links to division of labour in a facultatively eusocial sweat bee, Megalopta genalis. Queens are larger, have larger ovaries and have higher vitellogenin titres than workers. We then compared queens and workers with their solitary counterparts-solitary reproductive females and dispersing nest foundresses-to investigate physiological variation as a factor in caste evolution. Within dyads, body size and ovary development were the best predictors of behavioural class. Queens and dispersers are larger, with larger ovaries than their solitary counterparts. Finally, we raised bees in social isolation to investigate the influence of ontogeny on physiological variation. Body size and ovary development among isolated females were highly variable, and linked to differences in vitellogenin titres. As these are key physiological predictors of social caste, our results provide evidence for developmental caste-biasing in a facultatively eusocial bee.     

Methoprene accelerates age polyethism in workers of a social wasp (Polybia occidentalis)

Abstract. Topical applications of the Juvenile Hormone (JH) analogue methoprene to 1-day-old adult workers of the highly eusocial wasp Polybia occidentalis (Olivier) (Hymenoptera: Vespidae) accelerate the rate of age polyethism. Longevity of laboratory-reared wasps is negatively correlated with dose of topically applied methoprene. Doses of 25 μg methoprene or greater are lethal. Untreated wasps show marked age polyethism in the field. Age of first performance of acts in seven behavioural categories (in-nest, transition to outside, non-task on nest envelope, nest maintenance, foraged material handling, defence, and foraging) is negatively correlated with methoprene dose. Topical applications of methoprene accelerate age polyethism of highly eusocial bee and wasp workers, but do not have this effect on primitively eusocial bees and wasps, suggesting that JH control of age polyethism evolved independently in advanced species of Apidae and Vespidae.     

The effect of juvenile hormone on temporal polyethism in the paper wasp Polistes dominulus

Juvenile hormone (JH) has an important role in the behavior of eusocial Hymenoptera. Previous work has shown that JH influences aggression and dominance behavior in primitive eusocial insects that lack discrete queen and worker castes (e.g. Bombus bees and Polistes wasps). In contrast, JH is one of the factors that mediates temporal polyethism among workers in advanced eusocial insects that have reproductive castes (e.g. Apis bees and Polybiawasps). Therefore, initial observations suggest that JH may have different roles in primitive and advanced eusocial taxa. Here, we use detailed behavioral observations of marked individuals to test whether JH influences temporal polyethism in the primitive eusocial wasp Polistes dominulus. First, we show that workers in P. dominulus have an age-related division of labor, as workers switch from nest work to foraging as they mature. Then, we show that application of JH accelerates the onset of foraging behavior.Workers treated with JH start foraging at a younger age than control workers. Therefore, JH mediates temporal polyethism in the primitively eusocial insect Polistes dominulus. Received 23 April 2008; revised 6 August 2008; accepted 11 August 2008     

Honey bee queen mandibular pheromone inhibits ovary development and fecundity in a fruit fly

A key feature of eusocial insects is their reproductive division of labour. The queen signals her fecundity to her potentially reproductive daughters via a pheromone, which renders them sterile. In contrast, solitary insects lack division in reproductive labour and there is no such social signalling or need for ovary‐regulating pheromones. Nonetheless, females from both non‐social and eusocial lineages are expected to regulate their ovaries to maximize inclusive lifetime reproductive success. It is not known, however, whether the underlying networks that regulate ovary activation are homologous between non‐social and eusocial taxa, especially when these taxa are phylogenetically distant. In this study, we provide evidence that solitary fruit flies may share a conserved ovary‐regulating pathway with a eusocial honey bee, Apis mellifera L. (Hymenoptera: Apidae). Specifically, we demonstrate that honey bee queen mandibular pheromone (QMP) inhibits fly ovaries in much the same way as it suppresses worker ovaries. Drosophila melanogaster Meigen (Diptera: Drosophilidae) exposed to sufficient doses of QMP showed a reduction in ovary size, produced fewer eggs, and generated fewer viable offspring, relative to unexposed controls. Drosophila melanogaster therefore responds to an interspecific social cue to which it would not normally be exposed. Although we cannot strictly rule out an incidental effect, this conspicuous response suggests that these two species may share an underlying mechanism for ovary regulation. Why a non‐social species of fly responds to a highly social bee's pheromone is not clear, but one possibility is that solitary and social insects share pathways associated with female reproduction, as predicted by the ‘groundplan’ hypothesis of social evolution.     

Juvenile hormone in adult eusocial hymenoptera: Gonadotropin and behavioral pacemaker

Studies on the role of juvenile hormone (JH) in adult social Hymenoptera have focused on the regulation of two fundamental aspects of colony organization: reproductive division of labor between queens and workers and age-related division of labor among workers. JH acts as a gonadotropin in the primitively eusocial wasp and bumble bee species studied, and may also play this role in the advanced eusocial fire ants. However, there is no evidence that JH acts as a traditional gonadotropin in the advanced eusocial honey bee or in the few other ant species that have recently begun to be studied. The role of JH in age-related division of labor has been most thoroughly examined in honey bees. Results of these studies demonstrate that JH acts as a “behavioral pacemaker,” influencing how fast a worker grows up and makes the transition from nest activities to foraging. Hypotheses concerning the evolutionary relationship between the two functions of JH in adult eusocial Hymenoptera are discussed. Arch. Insect Biochem. Physiol. 35:559–583, 1997. © 1997 Wiley-Liss, Inc.     

Flexible task allocation and the organization of work in ants

Flexibility in task performance is essential for a robust system of division of labour. We investigated what factors determine which social insect workers respond to colony-level changes in task demand. We used radio-frequency identification technology to compare the roles of corpulence, age, spatial location and previous activity (intra-nest/extra-nest) in determining whether worker ants (Temnothorax albipennis) respond to an increase in demand for foraging or brood care. The less corpulent ants took on the extra foraging, irrespective of their age, previous activity or location in the nest, supporting a physiological threshold model. We found no relationship between ants that tended the extra brood and corpulence, age, spatial location or previous activity, but ants that transported the extra brood to the main brood pile were less corpulent and had high previous intra-nest activity. This supports spatial task-encounter and physiological threshold models for brood transport. Our data suggest a flexible task-allocation system allowing the colony to respond rapidly to changing needs, using a simple task-encounter system for generalized tasks, combined with physiologically based response thresholds for more specialized tasks. This could provide a social insect colony with a robust division of labour, flexibly allocating the workforce in response to current needs.     

Genetic variation and task specialization in the desert leaf-cutter ant, Acromyrmex versicolor

The genetic diversity in social insect colonies that is generated by multiple mating or multiple queens has been hypothesized to promote worker task specialization and therefore facilitate division of labour. However, few studies have actually examined the mechanisms by which genotype may influence individual worker behaviour. In this study, we dissect possible genetic effects on worker task performance in the desert leaf-cutter ant. We hypothesize that genotype could affect worker behaviour via (1) the rate of age-related task switching (age polyethism schedule), (2) individual task preference, and/or (3) task performance rates. To discriminate among these possible mechanisms, we generated composite colonies of workers from different genetic sources and followed the behaviour of individually marked workers over their lifetimes. We found significant differences among matrilines (offspring of different queens) in overall task performance. In particular, we found a negative covariance in likelihood of foraging versus tending fungus inside the nest. Workers of different matrilines also varied in the age of transition from inside the nest to foraging, but did not vary in task performance rates. Our results suggest that division of labour in this system is affected by genetic influences on individual task preference and age-related task choice, but not on variation in activity level.     

Dufour’s gland secretion,sterility and foraging behavior: Correlated behavior traits in bumblebee workers

Bombus terrestris colonies go through two major phases: the “pre-competition phase” in which the queen is the sole reproducer and aggression is rare, and the “competition phase” in which workers aggressively compete over reproduction. Conflicts over reproduction are partially regulated by a group of octyl esters that are produced in Dufour’s gland of reproductively subordinate workers and protect them from being aggressed. However, workers possess octyl esters even before overt aggression occurs, raising the question of why produce the ester-signal before it is functionally necessary?In most insect societies, foragers show reduced aggression and low dominance rank. We hypothesize that ester production in B. terrestris is not only correlated with sterility but also with foraging, signaling cooperative behavior by subordinate workers. Such a signal helps to maintain social organization, reduce the cost of fights between reproductives and helpers, and increase colony productivity, enabling subordinates to gain greater inclusive fitness. We demonstrate that foragers produce larger amounts of esters compared to non-foragers, and that their amounts positively correlate with foraging efforts. We further suggest that task performance, potential fecundity, and aggression are interlinked, and that worker–worker interactions are involved in regulating foraging behavior.B. terrestris, being an intermediate phase between primitive and derived eusocial insects, provides an excellent model for understanding the evolution of early phases of eusociality. Our results, combined with those in primitively eusocial wasps, suggest that at early stages of social evolution, reproduction was regulated by a “primordial division of labor”, that comprised foragers and reproducers, which further evolved to a more complex division of labor, a hallmark of eusociality.     

Developmental and dominance-associated differences in mushroom body structure in the paper wasp Mischocyttarus mastigophorus

Primitively eusocial paper wasps exhibit considerable plasticity in their division of labor. Dominance interactions among nest mates play a strong role in determining the task performance patterns of adult females. We asked whether dominance status and task performance differences were associated with the development of subregions of the mushroom bodies (MB) of female Mischocyttarus mastigophorus queens and workers. We found that the MB calycal neuropils were better developed (relative to the Kenyon cell body layer) in the dominant females that spent more time on the nest. Increased MB calyx development was more strongly associated with social dominance than with high rates of foraging. The MB of queens resembled those of dominant workers. The results suggest that social interactions are particularly relevant to M. mastigophorus females' cognition. By examining the MB of newly emerged females, we also found evidence for significant age-related changes in MB structure.     

Division of labor in post-emergence colonies of the primitively eusocial waspPolistes instabilis de Saussure (Hymenoptera: Vespidae)

Polyethism was quantified in post-emergence colonies of the primitively eusocial wasp,Polistes instabilis, and compared to polyethism in a sympatric advanced eusocial wasp,Polybia occidentalis. Like P.occidentalis, P. instabilis foragers collected food (nectar and prey) and nest materials (wood pulp and water).P. instabilis foragers showed some evidence of specialization with respect to which materials they gathered, but most foragers, divided their effort among food and nest materials, a pattern that is rarely seen inP. occidentalis. In colonies of both species, more foragers collected nectar than any other material; in contrast, most water foraging was performed by one or two workers. Upon returning to the nest,P. instabilis foragers gave up part or all of most nectar, prey, and pulp loads to nestmates, while water was rarely partitioned. Prey loads were most likely to be given up entirely.P. instabilis workers show evidence of conflict over the handling of materials at the nest. The frequency with which workers took portions of nectar loads from forgers was positively correlated with their frequency of aggressive dominant behavior, and with their frequency of taking other foraged materials. Compared to polyethism inP. occidentalis P. instabilis showed less individual specialization on foraging tasks and less partitioning of foraged materials with nestmates, suggesting that these characteristics of polyethism have been modified during the evolution of advanced insect societies.     

Inter‐individual variation in honey bee dance intensity correlates with expression of the foraging gene

Individual behavioural differences in responding to the same stimuli is an integral part of division of labour in eusocial insect colonies. Amongst honey bee nectar foragers, individuals strongly differ in their sucrose responsiveness, which correlates with strong differences in behavioural decisions. In this study, we explored whether the mechanisms underlying the regulation of foraging are linked to inter‐individual differences in the waggle dance activity of honey bee foragers. We first quantified the variation in dance activity amongst groups of foragers visiting an artificial feeder filled consecutively with different sucrose concentrations. We then determined, for these foragers, the sucrose responsiveness and the brain expression levels of three genes associated with food search and foraging; the foraging gene Amfor, octopamine receptor gene AmoctαR1 and insulin receptor AmInR‐2. As expected, foragers showed large inter‐individual differences in their dance activity, irrespective of the reward offered at the feeder. The sucrose responsiveness correlated positively with the intensity of the dance activity at the higher reward condition, with the more responsive foragers having a higher intensity of dancing. Out of the three genes tested, Amfor expression significantly correlated with dance activity, with more active dancers having lower expression levels. Our results show that dance and foraging behaviour in honey bees have similar mechanistic underpinnings and supports the hypothesis that the social communication behaviour of honey bees might have evolved by co‐opting behavioural modules involved in food search and foraging in solitary insects.     

The evolution of activity breaks in the nest cycle of annual eusocial bees: a model of delayed exponential growth

Background  

Social insects show considerable variability not only in social organisation but also in the temporal pattern of nest cycles. In annual eusocial sweat bees, nest cycles typically consist of a sequence of distinct phases of activity (queen or workers collect food, construct, and provision brood cells) and inactivity (nest is closed). Since the flight season is limited to the time of the year with sufficiently high temperatures and resource availability, every break reduces the potential for foraging and, thus, the productivity of a colony. This apparent waste of time has not gained much attention.     

Worker connectivity: a review of the design of worker communication systems and their effects on task performance in insect societies

Within-group communication is a fundamental feature of animal societies. In order for animal groups to function as adaptive units, the members must share information such that group mates respond appropriately to each others’ behavior. One important function of social communication is to affect the allocation of tasks among group members. Theoretical and empirical findings on a diverse array of social insect taxa show that interactions among workers often play important roles in structuring division of labor. We review worker interactions that regulate division of labor in insect societies, which we refer to as worker connectivity. We present a framework for synthesizing and analyzing the study of worker connectivity. The widespread reliance on worker connectivity among eusocial insect taxa and the diversity of communicative mechanisms used to recruit workers suggest that the nature of worker interactions has evolved by natural selection. We suggest that colony-level selection acting on variation in task allocation has been an important force in the evolution of mechanisms for worker connectivity. We also propose that there are important links between individual worker cognition and task allocation at the colony level. Evolutionary changes in the cognitive aspects of worker responses may affect task allocation as much as changes in the communicative signals themselves. Received 9 December 2006; revised 18 May 2007; accepted 30 May 2007.     

Hierarchical networks of food exchange in the black garden ant Lasius niger

In most eusocial insects, the division of labor results in relatively few individuals foraging for the entire colony. Thus, the survival of the colony depends on its efficiency in meeting the nutritional needs of all its members. Here, we characterize the network topology of a eusocial insect to understand the role and centrality of each caste in this network during the process of food dissemination. We constructed trophallaxis networks from 34 food-exchange experiments in black garden ants (Lasius niger). We tested the influence of brood and colony size on (i) global indices at the network level (i.e., efficiency, resilience, centralization, and modularity) and (ii) individual values (i.e., degree, strength, betweenness, and the clustering coefficient). Network resilience, the ratio between global efficiency and centralization, was stable with colony size but increased in the presence of broods, presumably in response to the nutritional needs of larvae. Individual metrics highlighted the major role of foragers in food dissemination. In addition, a hierarchical clustering analysis suggested that some domestics acted as intermediaries between foragers and other domestics. Networks appeared to be hierarchical rather than random or centralized exclusively around foragers. Finally, our results suggested that networks emerging from social insect interactions can improve group performance and thus colony fitness.