Dominance and polyethism in the eusocial wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Dominance interactions affected patterns of non-reproductive division of labor (polyethism) in the eusocial wasp Mischocyttarus mastigophorus. Socially dominant individuals foraged for food (nectar and insect prey) at lower rates than subordinate individuals. In contrast, dominant wasps performed most of the foraging for the wood pulp used in nest construction. Social dominance also affected partitioning of materials collected by foragers when they returned to the nest. Wood pulp loads were never shared with nest mates, while food loads, especially insect prey, were often partitioned with other wasps. Dominant individuals on the nest were more likely to take food from arriving foragers than subordinate individuals. The role of dominance interactions in regulating polyethism has evolved in the eusocial paper wasps (Polistinae). Both specialization by foragers and task partitioning have increased from basal genera (independent-founding wasps, including Mischo-cyttarus spp.) to more derived genera (swarm-founding Epiponini). Dominance interactions do not regulate forager specialization or task partitioning in epiponines. I hypothesize that these changes in polyethism were enabled by the evolution of increased colony size in the Epiponini. Received: 8 December 1997 / Accepted after revision: 28 March 1998     

Genotypic variability in age polyethism and task specialization in the honey bee,Apis mellifera (Hymenoptera: Apidae)

Summary The currently accepted model for division of labor in honey bees, Apis mellifera, explains variation in the frequency at which workers perform specific tasks as the result of differences in age and environment. Although well documented, the model is incomplete because it fails to take genotypic variability among workers into account. We show that workers from two genetically distinct strains of honey bees differed in the age at which they began foraging and in the relative frequency at which they foraged for pollen. Workers from the two strains also exhibited significant spatial heterogeneity within the nest, suggesting that they differed in the frequency at which they performed within-nest tasks as well. A heuristic model of division of labor that incorporates genotypic effects is presented.     

Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor

The daily patterns of task performance in honey bee colonies during behavioral development were studied to determine the role of circadian rhythmicity in age-related division of labor. Although it is well known that foragers exhibit robust circadian patterns of activity in both field and laboratory settings, we report that many in-hive tasks are not allocated according to a daily rhythm but rather are performed 24 h per day. Around-the-clock activity at the colony level is accomplished through the performance of some tasks by individual workers randomly with respect to time of day. Bees are initially arrhythmic with respect to task performance but develop diel rhythmicity, by increasing the occurrence of inactivity at night, prior to becoming foragers. There are genotypic differences for age at onset of rhythmicity and our results suggest that these differences are correlated with genotypic variation in rate of behavioral development: genotypes of bees that progressed through the age polyethism schedule faster also acquired behavioral rhythmicity at an earlier age. The ontogeny of circadian rhythmicity in honey bee workers ensures that essential in-hive behaviors are performed around the clock but also allows the circadian clock to be engaged before the onset of foraging. Received: 6 October 1997 / Accepted after revision: 28 March 1998     

Nesting success of rufous-naped wrens (Campylorhynchus rufinucha) is greater near wasp nests

Summary Rufous-naped wrens (Campylorhynchus rufinucha) in northwestern Costa Rica build breeding nests most frequently in ant-acacia trees (Acacia collinsii) and occasionally near wasp nests in ant-acacia trees. By moving occupied wasp nests (Polybia rejecta) to randomly chosen ant-acacia trees with wren nests, I tested the hypothesis that wrens nesting near wasp nests were more likely to fledge young than wrens not nesting near wasp nests. Wrens whose nests were near experimentally relocated wasp nests were significantly more likely to fledge young (37.5% of 16 attempts in 1987 and 75% of 12 attempts in 1988) than were wrens whose nests had no wasp nests placed near them (0% of 16 attempts in 1987 and 20% of 15 attempts in 1988). In 15 cases, repeated nesting attempts occurred in the same trees both with and without experimentally-placed wasp nests. Analysis of these data allowed a comparison of the effect of wasp nests on fledging success while differences among trees were controlled. Within the same tree, nesting attempts associated with wasp nests were significantly more likely to fledge young than nesting attempts without wasp nests. Predation was the primary cause of nest failure, and within forest, white-faced monkeys (Cebus capucinus) were the most important predators. The difference in success of wren nests with and without wasps and observations of predators indicate that enhancement of fledging success was due to deterrence of predatory vertebrates by wasps.     

Social organization in the ant Pheidole dentata

Summary Caste theory states that the proportions of individuals in different demographic classes of an insect society should vary with environmental factors, and are adaptive because they enhance colony-level efficiency. We examined the proportions of workers in different age and size classes (temporal and physical castes) in whole colonies of the ant Pheidole dentata collected in two different habitats. Despite significant ecological differences between the habitats in competition, resource availability and predation, we found no differences in the physical and temporal caste structures of colonies. Also, there was no correlation between physical or temporal caste ratios and the reproductive output of colonies. Because of topography, distance between sites, and apparent low vagility of Pheidole alates, we assume that gene flow between the sites is inadequate to account for the observed similarities. Although age- and size-related patterns of division of labor were observed, similarities in the behavioral profiles (the sum of the relative contributions of each age cohort to the performance of tasks) in colonies having different age caste structures suggests that worker, flexibility may be more important than rigidly programmed age- and size-correlated patterns of task performance.     

Division of labor and the evolution of task sharing in queen associations of the harvester ant<Emphasis Type="Italic"> Pogonomyrmex californicus</Emphasis>

Division of labor is a key factor in the ecological success of social groups. Recent work suggests that division of labor can emerge even without specific adaptations for task specialization and that it can appear in incipient social groups as a self-organizational property. We investigated experimentally how selection and self-organization may interact during the evolution of division of labor by examining task performance in groups of normally solitary versus normally social ant queens. We created social pairs of colony-founding queens from two populations of the ant Pogonomyrmex californicus, one in which queens are normally solitary and one in which queens form foundress groups, and observed their behavior during nest excavation. In both populations, one of the two queens usually performed most of the excavation, becoming the excavation specialist. We could predict which queen would become the specialist based on their relative propensities to perform the task in other contexts, consistent with a variance-based model of task specialization. The occurrence of specialization even when group members were not adapted to social life suggests that division of labor may well have been present in incipient queen groups. However, division of labor can result in cost skew among group members, and thus, paradoxically, within-group selection may constrain or even reduce specialization. Consistent with this effect, pairs of normally solitary queens were significantly more asymmetrical in their task performance than normally social pairs, in which both queens nearly always performed the behavior to some degree.Communicated by J. Heinze     

Queuing for dominance: gerontocracy and queue-jumping in the hover wasp <Emphasis Type="Italic">Liostenogaster flavolineata</Emphasis>

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.     

Work division of floral scent compounds in mediating pollinator behaviours

Floral scents are known as an olfactory signal for attracting pollinators, but why the flowers pollinated by highly specialised pollinators emit scents consisting of mixtures of many compounds and dominated by one or a few compounds is still poorly understood. We supposed that each (especially characteristic) chemical in floral scents may play a specific role in mediating pollinator behaviours and tested this supposition in a fig-fig wasp mutualism. Ficus curtipes is obligately pollinated by an undescribed Eupristina species. In the scent of F. curtipes receptive figs, over 50 compounds have been identified, and the scent is dominated by two compounds, 6-methyl-5-hepten-2-ol (OL) and 6-methyl-5-hepten-2-one (NE). We therefore tested the roles of the two major chemicals in mediating the pollinator behaviours. Our results show that OL and NE, respectively, act as a long-distance attractant and a fig-entry behaviour stimulant to the obligate pollinator wasp. Namely, OL attracts the wasps to the figs and NE guides the wasps into the figs. This finding on the work division of floral scent compounds partially explains the maintenance mechanism of the fig-fig wasp mutualism and the significance of the chemical diversity of floral scent in plant–pollinator interactions, especially in specialised pollination systems.     

RAPD markers suggest genotypic effects on forager specialization in a eusocial wasp

Genetic variability within insect societies may provide a mechanism for increasing behavioral diversity among workers, thereby augmenting colony efficiency or flexibility. In order to assess the possibility that division of labor has a genetic component in the eusocial wasp Polybia aequatorialis, I asked whether the genotypes of workers within colonies correlated with behavioral specialization. Workers specialized by foraging for one of the four materials (wood pulp, insect prey, nectar, or water) gathered by their colonies. I collected foragers on 2 days from each of three colonies and identified the material the foragers were carrying when collected. I produced random amplified polymorphic DNA (RAPD) markers from the genomic DNA of these foragers and estimated genotypic similarity of foragers based on sharing of variable RAPD marker bands. Contingency tests on 20 variable loci per colony showed statistically significant (P <0.05) biases in RAPD marker frequencies among forager types in the three colonies. Patterns of association of RAPD marker bands with specializations were constant in two colonies, but changed between collection days in one colony. RAPD marker biases suggest that division of labor among workers includes a genetic component in P. aequatorialis. Colony-level selection on variation in division of labor is a possible factor favoring the evolutionary maintenance of high genotypic variability (low relatedness) in epiponine wasp colonies and in other eusocial insects. Received: 18 July 1995/Accepted after revision: 1 October 1995     

Regulation of honey bee age polyethism by juvenile hormone

Summary Previous studies suggested that juvenile hormone (JH) is involved in the regulation of physiological processes that are associated with division of labor in honey bees but the effects of JH on behavior were not clear. The hypothesis that JH affects worker age polyethism was tested by observing individually marked bees topically treated with different doses of the JH analog methoprene. Methoprene caused dose-dependent changes in the timing and frequency of occurrence of four important age-dependent tasks: brood and queen care, food storage, nest maintenance, and foraging. Weak or no effects were observed for social interactions, self-grooming, and other non-task behaviors that were not performed in an age-dependent manner. These results support the hypothesis that JH is involved in the control of age polyethism. A model is presented that explains the role of JH in regulating division of labor. JH may regulate the colony's allocation of labor by altering the probabilities of response to tasks. According to this model, hormone titers increase with age according to a genetically determined pattern of development, but this rise may be modulated by environmental and colony factors such as food availability and population structure. Extrinsic regulation of JH may be a mechanism underlying the ability of workers to respond to changing colony needs.     

The ability of conditioned Microplitis croceipes (Hymenoptera: Braconidae) to distinguish between odors of aflatoxigenic and non-aflatoxigenic fungal strains

Summary. The parasitic wasp Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) learns to associate odors with food resources and subsequently exhibits a characteristic food-seeking behavior when encountering the learned odor. Wasps so conditioned, learned and subsequently demonstrated an ability to distinguish among aflatoxigenic and non-aflatoxigenic Aspergillus flavus and A. parasiticus strains. The effects of fungal species, strain, age (5, 10-12, 20, and 30 d) and growth media (potato dextrose agar, peanut agar and corn agar) on the learning and recognition responses of the conditioned wasps were examined. The level of differentiation between fungal strains by conditioned wasps was lowest when working with 5-d-old fungal cultures but increased with age and generally peaked with 20-d-old fungi. Wasps responded generally stronger to the fungal strain conditioned to independent of growth media. This ability of parasitic wasps to learn and distinguish fungal odors can open new avenues in insect learning.     

Exploitation of carbohydrate food sources in <Emphasis Type="Italic">Polybia occidentalis</Emphasis>: social cues influence foraging decisions in swarm-founding wasps

An efficient exploitation of carbohydrate food sources would be beneficial for social wasp species that store nectar within their nest. In the swarm-founding polistine wasp Polybia occidentalis, we now demonstrate that the decisions of when and where to forage are influenced by information from conspecifics. Only when foragers had been trained to collect at artificial carbohydrate feeders did newcomers (food-source-naive individuals) continuously arrive at these feeders during 2 h of experiment. In control tests, in which no forager had been trained, not a single newcomer alighted at any of the offered carbohydrate food sources. This indicates that, during the foraging process, a nest-based input provided by successful foragers must have stimulated nestmates to search for food. Once activated, the newcomers’ choice on where to collect was strongly influenced by field-based social information. The mere visual presence of accumulated conspecifics (wasp dummies placed on one of the feeders) attracted newcomers to the food sources. Interestingly, however, visual enhancement was not the only decision-biasing factor at the feeding site. In an experimental series where searching wasps had to choose between the experimental feeder at which 3 foragers continuously collected and the control feeder with nine wasp dummies, only 40% of the wasps chose the visually enhanced feeder. This points to the existence of additional mechanisms of local enhancement. The possibility that, in social wasps, recruitment is involved in the exploitation of carbohydrate food sources is discussed.     

Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants

The controversy concerning the extent to which the organization of division of labor in social insects is a developmental process or is based on task allocation dynamics that emerge from colony need independent of worker age and endocrine or neural state has yet to be resolved. We present a novel analysis of temporal polyethism in the ant Pheidole dentata, demonstrating that task attendance by minor workers does not shift among spatially associated sets of behaviors that minimally overlap but rather expands with age. Our results show that the number of tasks performed by older minors increases through the addition and retention of behaviors, with up to a sixfold increase in repertoire size from day 1 to day 20 of adult life. We also show that older minors respond to colony needs by performing significantly more brood care as its demand increases, indicating that they can quickly upregulate nursing according to labor requirements. This level of plasticity was absent in younger siblings. The breadth of responsiveness to task-related olfactory stimuli increased with age. In a binary choice test in which young and old minor workers could orient toward odorants from brood or food, older workers responded to both brood and food, whereas young workers responded only to brood. These dissimilar responses to stimuli associated with nursing and foraging indicate age-related differences in sensory ability and provide a physiological basis for the age-related repertoire expansion model. We discuss repertoire expansion in P. dentata in light of behavioral development and caste flexibility in ants.     

Weak specialization of workers inside a bumble bee (<Emphasis Type="Italic">Bombus impatiens</Emphasis>) nest

Division of labor is common across social groups. In social insects, many studies focus on the differentiation of in-nest and foraging workers and/or the division of foraging tasks. Few studies have specifically examined how workers divide in-nest tasks. In the bumble bee, Bombus impatiens, we have shown previously that smaller workers are more likely to feed larvae and incubate brood, whereas larger workers are more likely to fan or guard the nest. Here, we show that in spite of this, B. impatiens workers generally perform multiple tasks throughout their life. The size of this task repertoire size does not depend on body size, nor does it change with age. Further, individuals were more likely to perform the task they had been performing on the previous day than any other task, a pattern most pronounced among individuals who guarded the nest. On the other hand, there was no predictable sequence of task switching. Because workers tend to remain in the same region of the nest over time, in-nest workers may concentrate on a particular task, or subset of tasks, inside that region. This division of space, then, may be an important mechanism that leads to this weak specialization among in-nest bumble bee workers.     

Evolution of self-organized division of labor in a response threshold model

Division of labor in social insects is determinant to their ecological success. Recent models emphasize that division of labor is an emergent property of the interactions among nestmates obeying to simple behavioral rules. However, the role of evolution in shaping these rules has been largely neglected. Here, we investigate a model that integrates the perspectives of self-organization and evolution. Our point of departure is the response threshold model, where we allow thresholds to evolve. We ask whether the thresholds will evolve to a state where division of labor emerges in a form that fits the needs of the colony. We find that division of labor can indeed evolve through the evolutionary branching of thresholds, leading to workers that differ in their tendency to take on a given task. However, the conditions under which division of labor evolves depend on the strength of selection on the two fitness components considered: amount of work performed and on worker distribution over tasks. When selection is strongest on the amount of work performed, division of labor evolves if switching tasks is costly. When selection is strongest on worker distribution, division of labor is less likely to evolve. Furthermore, we show that a biased distribution (like 3:1) of workers over tasks is not easily achievable by a threshold mechanism, even under strong selection. Contrary to expectation, multiple matings of colony foundresses impede the evolution of specialization. Overall, our model sheds light on the importance of considering the interaction between specific mechanisms and ecological requirements to better understand the evolutionary scenarios that lead to division of labor in complex systems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-012-1343-2) contains supplementary material, which is available to authorized users.     

Interspecific interference competition and mate choice in the soldier beetle,Chauliognathus pennsylvanicus

Summary Interference competition directed at soldier beetles, Chauliognathus pennsylvanicus, by four aggressive wasp species changed the mate choice of females. In the absence of wasps, females mated more frequently with males of greater weight and greater antennal scape diameter. Only in the presence of wasps did females frequently mate when they did not contain mature ova. When wasps were abundant, the proportion of beetles mating was higher. Wasps reacted aggressively toward mating beetles less frequently than toward single beetles. Therefore, females may have fed more efficiently in the presence of wasps when coupled.     

Local mate competition in the solitary parasitoid wasp <Emphasis Type="Italic">Ooencyrtus kuvanae</Emphasis>

Local mate competition (LMC) occurs when brothers compete with each other for mating opportunities, resulting in selection for a female-biased sex ratio within local groups. If multiple females oviposit in the same patch, their sons compete for mating opportunities with non-brothers. Females, in the presence of other females, should thus produce relatively more sons. Sex ratio theory also predicts a more female-biased sex ratio when ovipositing females are genetically related, and sex-ratio responses to foundress size if it differentially affects fitness gains from sons versus daughters. The mating system of the parasitoid wasp Ooencyrtus kuvanae meets assumptions of LMC. Females insert a single egg into each accessible egg of gypsy moth, Lymantria dispar, host egg masses. Wasps complete development inside host eggs and emerge en masse, as sexually mature adults, resulting in intense competition among brothers. We tested the hypothesis that O. kuvanae exhibits LMC by manipulating the number of wasp foundresses on egg masses with identical numbers of eggs. As predicted by LMC theory, with increasing numbers of wasp foundresses on an egg mass, the proportions of emerging sons increased. In contrast, the presence of a sibling compared to a non-sibling female during oviposition, or the size of a female, did not affect the number or sex ratio of offspring produced. The O. kuvanae system differs from others in that larvae do not compete for local resources and thus do not distort the sex ratio in favor of sons. With no resource competition among O. kuvanae larvae, the sex ratio of emergent son and daughter wasps is due entirely to the sex allocation by ovipositing wasp foundresses on host egg masses.     

Aging and demographic plasticity in response to experimental age structures in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L)

Honeybee colonies are highly integrated functional units characterized by a pronounced division of labor. Division of labor among workers is mainly age-based, with younger individuals focusing on in-hive tasks and older workers performing the more hazardous foraging activities. Thus, experimental disruption of the age composition of the worker hive population is expected to have profound consequences for colony function. Adaptive demography theory predicts that the natural hive age composition represents a colony-level adaptation and thus results in optimal hive performance. Alternatively, the hive age composition may be an epiphenomenon, resulting from individual life history optimization. We addressed these predictions by comparing individual worker longevity and brood production in hives that were composed of a single-age cohort, two distinct age cohorts, and hives that had a continuous, natural age distribution. Four experimental replicates showed that colonies with a natural age composition did not consistently have a higher life expectancy and/or brood production than the single-cohort or double-cohort hives. Instead, a complex interplay of age structure, environmental conditions, colony size, brood production, and individual mortality emerged. A general tradeoff between worker life expectancy and colony productivity was apparent, and the transition from in-hive tasks to foraging was the most significant predictor of worker lifespan irrespective of the colony age structure. We conclude that the natural age structure of honeybee hives is not a colony-level adaptation. Furthermore, our results show that honeybees exhibit pronounced demographic plasticity in addition to behavioral plasticity to react to demographic disturbances of their societies.     

Emergence of increased division of labor as a function of group size

Empirical evidence suggests that division of labor in insect societies is positively related to group size both within and across taxa. Response threshold models (RTM) have been commonly used to analyze patterns of division of labor. However, these models have been explored empirically and theoretically for only a limited number of tasks, and few studies have examined predictions of the model as colony size and work availability change. We theoretically examine how group size influences division of labor using a fixed response-threshold model. We simultaneously explore how expected by-products of increased colony size, including demand (total work need relative to total work force available) and task number, affect this relationship. Our results indicate that both low demand and high task number positively influence division of labor. We suggest that these changes parallel what is observed within social groups as their size increases, and that, in part, the commonly observed increased division of labor with increasing group size is emergent.     

Adaptive responses to local mate competition by the parasitoid,Telenomus remus

Summary The parasitic wasp, Telenomus remus, lays her eggs in diserete patches of moth eggs, where her offspring develop and mate before dispersal, satisfying conditions for local mate competition (LMC). In the presence of other ovipositing females, wasps lay a higher sex ratio (proportion males), as predicted by LMC theory, and achieve this by a combination of two mechanisms, (1) avoidance of superparasitism and a sequence of sex allocation initially biased towards males and (2) a direct increase in sex ratio in the presence of other wasps, sex ratio increases with the proportion of previously parasitized hosts, as predicted by LMC theory. In both cases, chemical traces left by foraging wasps are indicated as the stimuli causing wasps to increase the proportion of males allocated to hosts.