Influence of caste polyethism on longevity of workers in social insect colonies

Different patterns of division of labor can affect the expected longevity of social insects workers. It has been earlier suggested that when tasks performed inside and outside colony are equally risky then the expected longevity of workers in colonies with caste polyethism is greater than that in colonies without polyethism. To verify these predictions I used a model assuming two sets of tasks, associated with different mortality rates. In the colony without polyethism the workers preformed safe and risky tasks in turn, while in the colony with caste polyethism the workers specialized in only one set of tasks. The outcomes suggest that the expected longevity of workers in colonies with caste polyethism cannot be greater than that in colonies without polyethism. Only if there is no aging and under some special and rare conditions are there no differences in expected longevity between colonies with and without caste polyethism. If aging is independent of activity, caste polyethism does not shorten longevity when all tasks in the colony are equally risky. The results can explain why caste polyethism is not as widespread among social insects as age polyethism.     

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     

Genetic effects on task performance,but not on age polyethism,in a swarm-founding eusocial wasp

Division of labour among workers in insect societies often includes two major components: age-related changes in behaviour (age polyethism) and specialization in task performance. The aim of this study was to test whether similarity in inside-nest task performance and in rate of age polyethism correspond to genetic similarity among nestmates in the polygynous eusocial waspPolybia aequatorialis.Behavioural data were collected on marked, known-age workers from three source colonies introduced into two observation colonies in the field. Genetic similarity among workers was assessed by quantifying sharing of random amplified polymorphic DNA (RAPD) marker alleles. Workers were categorized by whether they engaged in nest cleaning as an indicator of individual differences in inside-nest task performance. Within source colonies, workers that performed nest-cleaning tasks were more genetically similar to each other than they were to workers not performing these tasks. Workers also differed in their rates of passage through the age-related task sequence, but no association was found between sharing of RAPD marker alleles and rate of age polyethism. These results accord with earlier studies demonstrating flexibility in age polyethism in swarm-founding wasps, and with findings that worker genotypic variability corresponds to specialization in task performance inP. aequatorialis. Polybiaspp. workers rarely switch among tasks, even in response to changes in colony conditions, and workers’ genotypes may constrain flexibility in task performance at the individual level. Conversely, colonies may accrue benefits from having genotypically diverse worker forces, which could favour the maintenance of polygyny in swarm-founding wasps.     

Social inhibition and the regulation of temporal polyethism in honey bees.

Honey bee division of labor is characterized by temporal polyethism, in which young workers remain in the hive and perform tasks there, whereas old workers perform more risky outside tasks, mainly foraging. We present a model of honey bee division of labor based on (1) an intrinsic process of behavioral development and (2) inhibition of development through social interactions among the workers in a colony. The model shows that these two processes can explain the main features of honey bee temporal polyethism: the correlation between age and task performance; the age at which a worker first forages and how this age varies among hives; the balanced allocation of workers to hive tasks and foraging; the recovery of a colony from demographic perturbations; and the differentiation of workers into different behavioral roles. The model provides a baseline picture of individual and colony behavior that can serve as the basis for studies of more fine-grained regulation of division of labor.     

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.     

Flexible division of labor mediated by social interactions in an insect colony-a simulation model

The primitively eusocial wasp Ropalidia marginata shows an age-based division of labor in which workers allocate tasks according to their relative ages (age ranks). This age polyethism seems quite flexible because in colonies devoid of old workers, young individuals can perform the tasks normally performed by older workers. Social interactions appear to be a plausible mechanism by which workers can assess their relative ages. To explore possible proximate mechanisms that can potentially generate such a flexible, age-based task allocation, the activator-inhibitor model was adapted to the social biology of R. marginata and tested using computer simulations. The model generated a clear age polyethism including the phenomena of precocious foragers in colonies with only young individuals and reverted nurses in colonies consisting of only old individuals. A simple extension of the model to allow the brood:adult ratio to modulate the rates of social interactions, shows how increasing task demands can be met by a decrease in the ages of first performance of, and an increase in the proportions of individuals engaged in, various tasks. These results show how a pattern of division of labor based on relative age can be generated and modulated by social interactions. Copyright 1999 Academic Press.     

Juvenile hormone accelerates ovarian development and does not affect age polyethism in the primitively eusocial wasp,Ropalidia marginata

Juvenile hormone modulates post-imaginal reproductive division of labor in primitively eusocial species and promotes the production of queens (e.g., Polistes) while it modulates age polyethism and promotes the production of foragers in highly eusocial species (e.g., the honey bee). Ropalidia marginata is a primitively eusocial wasp that shows both post-imaginal regulation of reproductive division of labor as well as age polyethism. Hence, R.marginata is a particularly interesting model system to study the effect of juvenile hormone. We demonstrate here that a single, topical application of 100 micro g of juvenile hormone-III per female wasp accelerates ovarian development of wasps held in isolation. Similar application to wasps released back on to their natal nests has no effect on their rate of behavioral development as witnessed from the age of first performance of feed larva, build, bring pulp and bring food. We conclude therefore that in R.marginata, juvenile hormone has retained its function of modulating reproductive division of labor and has not acquired the function of modulating age polyethism.     

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.     

Shorter-lived workers start foraging earlier

In social insects it is often observed that young workers perform tasks inside the nest and later switch to tasks outside the nest. By doing this the workers maximize their expected longevity, because tasks inside the nest are safe and tasks outside the nest are risky. The optimal strategy of workers should be expected to depend not only on their age but also on their health status if it is associated with reduction of longevity. Here a mathematical model is used to calculate the optimal time of switching between safe and risky tasks in a colony consisting of both healthy and unhealthy workers. The model predicts that unhealthy workers, with shorter longevity, should perform more risky tasks at an earlier age than their healthy nest mates should. The optimal time to switch between safe and risky tasks depends on the proportion of healthy and unhealthy workers in the colony, but the workers need not perceive the health status of their nest mates in order to adopt the optimal strategy. The workers need only perceive their own life expectancy, because the life expectancy of healthy and unhealthy workers should be the same at the time of switching from safe to risky tasks. The model predictions agree with a wide range of empirical data presented in this paper. Workers that are infected, poisoned, injured or affected by other harmful factors start to forage and perform other risky tasks at an earlier age than their healthy nest mates.     

The curious case of aging plasticity in honey bees

As in all advanced insect societies, colony-organization in honey bees emerges through a structured division of labor between essentially sterile helpers called workers. Worker bees are sisters that conduct all social tasks except for egg-laying, for example nursing brood and foraging for food. Curiously, aging progresses slowly in workers that engage in nursing and even slower when bees postpone nursing during unfavorable periods. We, therefore, seek to understand how senescence can emerge as a function of social task performance. The alternative utilization of a common yolk precursor protein (vitellogenin) in nursing and somatic maintenance can link behavior and aging plasticity in worker bees. Beneficial effects of vitellogenin may also be mediated by inhibitory action on juvenile hormone and insulin-like signaling.     

Age polyethism in the leaf-cutting ant Acromyrmex subterraneus brunneus Forel, 1911 (Hym., Formicidae)

Abstract  This study describes and quantifies the behavioural acts of two laboratory colonies of Acromyrmex subterraneus brunneus by investigating worker age polyethism. Twenty-nine behavioural acts were recorded during the 19-week observation period. Young individuals performed tasks inside the nest related to brood care and care for the fungus garden, whereas older individuals performed activities outside the nest such as foraging and activities in the waste chamber. The average longevity (±SD) was 108.21 ± 3.30, 109.15 ± 1.92 and 122.71 ± 1.55 days for large, medium and small workers, respectively. The small-sized workers presented a higher probability of reaching older age than large- and medium-sized workers. This study describes task switching according to age polyethism and the relationship of physical and temporal subcastes.     

Polyethism and the adaptiveness of worker size variation in the attine antTrachymyrmex septentrionalis

Division of labor was studied in colonies from Long Island and Florida populations of the fungus-gardening antTrachymyrmex septentrionalis. Workers showed age polyethism and a weak size polyethism, and these patterns of division of labor were not different in colonies from the two populations. Individual workers had repertoires comprised of three to five roles but tended to concentrate their labor within a single role. The data are consistent with the hypothesis that worker polymorphism and the elaboration of size-related behavior in the attine ants evolved along with the use of fresh vegetation as the fungal substrate. The data do not support the hypothesis that size variation in colonies ofT. septentrionalis evolved to promote efficient division of labor. Division of labor within the worker caste is based mainly on age and appears to be an attribute of the species rather than an adaptation to a particular habitat.     

蜜蜂群内生殖分工体系的形成及其维持

本文对蜜蜂群内生殖分工体系的形成及其维持机制进行综述。蜜蜂群体具有完善的劳动分工(包括生殖分工)体系,蜂王垄断生殖权力,而工蜂生殖器官发育不完全,在蜂王信息素和幼虫信息素的作用下产卵受到抑制。蜂王的多雄交配机制降低了群内个体间的亲缘关系,但也促进了工蜂间相互监督机制的形成。工蜂间的相互监督,结合蜂王和幼虫信息素对工蜂卵巢发育的影响,解决了蜂王与工蜂、工蜂与工蜂间的生殖利益冲突,保障了蜂群内的生殖分工体系,提高了群体效率,维护了蜂群的真社会性。     

Age- and subcaste-related patterns of serotonergic immunoreactivity in the optic lobes of the ant Pheidole dentata

Serotonin, a biogenic amine known to be a neuromodulator of insect behavior, has recently been associated with age-related patterns of task performance in the ant Pheidole dentata. We identified worker age- and subcaste-related patterns of serotonergic activity within the optic lobes of the P. dentata brain to further examine its relationship to polyethism. We found strong immunoreactivity in the optic lobes of the brains of both minor and major workers. Serotonergic cell bodies in the optic lobes increased significantly in number as major and minor workers matured. Old major workers had greater numbers of serotonergic cell bodies than minors of a similar age. This age-related increase in serotonergic immunoreactivity, as well as the presence of diffuse serotonin networks in the mushroom bodies, antennal lobes, and central complex, occurs concomitantly with an increase in the size of worker task repertoires. Our results suggest that serotonin is associated with the development of the visual system, enabling the detection of task-related stimuli outside the nest, thus playing a significant role in worker behavioral development and colony-wide division of labor.     

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.     

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.     

Expression of the Foraging Gene Is Associated with Age Polyethism,Not Task Preference,in the Ant Cardiocondyla obscurior

One of the fundamental principles of social organization, age polyethism, describes behavioral maturation of workers leading to switches in task preference. Here we present a system that allows for studying division of labor (DOL) by taking advantage of the relative short life of Cardiocondyla obscurior workers and thereby the pace of behavioral transitions. By challenging same-age young and older age cohorts to de novo establish DOL into nurse and foraging tasks and by forcing nurses to precociously become foragers and vice versa we studied expression patterns of one of the best known candidates for social insect worker behavior, the foraging gene. Contrary to our expectations we found that foraging gene expression correlates with age, but not with the task foraging per se. This suggests that this nutrition-related gene, and the pathways it is embedded in, correlates with physiological changes over time and potentially primes, but not determines task preference of individual workers.     

Senescence in the worker honey bee Apis Mellifera

Honey bees are social insects that exhibit striking caste-specific differences in longevity. Queen honey bees live on average 1-2 years, whereas workers live 2-6 weeks in the summer and about 20 weeks in the winter. It is not clear whether queen-worker differences in longevity are due to intrinsic physiological differences in the rate of senescence, to differential exposure to extrinsic factors such as predation and adverse environmental conditions, or both. To determine if the relatively short lifespan of worker bees involves senescence, we measured age-specific resistance to three different physiological stressors (starvation, thermal, and oxidative stress) while eliminating age-related differences in foraging activity and minimizing age-related differences in energy expenditure. Despite these manipulations, older worker bees were still significantly less resistant to all three stressors than were younger bees. These results indicate that the regulation of worker bee lifespan involves senescence, in addition to extrinsic factors.     

Effects of selection for honey bee worker reproduction on foraging traits

The “reproductive ground plan” hypothesis (RGPH) proposes that reproductive division of labour in social insects had its antecedents in the ancient gene regulatory networks that evolved to regulate the foraging and reproductive phases of their solitary ancestors. Thus, queens express traits that are characteristic of the reproductive phase of solitary insects, whereas workers express traits characteristic of the foraging phase. The RGPH has also been extended to help understand the regulation of age polyethism within the worker caste and more recently to explain differences in the foraging specialisations of individual honey bee workers. Foragers that specialise in collecting proteinaceous pollen are hypothesised to have higher reproductive potential than individuals that preferentially forage for nectar because genes that were ancestrally associated with the reproductive phase are active. We investigated the links between honey bee worker foraging behaviour and reproductive traits by comparing the foraging preferences of a line of workers that has been selected for high rates of worker reproduction with the preferences of wild-type bees. We show that while selection for reproductive behaviour in workers has not altered foraging preferences, the age at onset of foraging of our selected line has been increased. Our findings therefore support the hypothesis that age polyethism is related to the reproductive ground plan, but they cast doubt on recent suggestions that foraging preferences and reproductive traits are pleiotropically linked.     

Foraging for Work and Age-Based Polyethism: The Roles of Age and Previous Experience on Task Choice in Ants

In social insects, colonies commonly show temporal polyethism in worker behavior, such that a worker follows a predictable pattern of changes between tasks as it ages. This pattern usually leads from workers first doing a safe task like brood care, to ending their lives doing the most dangerous tasks like foraging. Two mechanisms could potentially underlie this pattern: (1) age‐based task allocation, where the aging process itself predisposes workers to switch to more dangerous tasks; and (2) foraging for work, where ants switch to tasks that need doing from tasks which have too many associated workers. We tested the relative influence of these mechanisms by establishing nests of Camponotus floridanus with predetermined combinations of workers of known age and previous task specialization. The results supported both mechanisms. Nests composed of entirely brood‐tending workers had the oldest workers preferentially switching to foraging. However, in nests initially composed entirely of foragers, the final distribution of tenders and foragers was not different from random task‐switching and therefore supportive of foraging for work. Thus, it appears that in C. floridanus there is directionality to the mechanisms of task allocation. Switching to more dangerous tasks is age‐influenced, but switching to less dangerous tasks is age‐independent. The results also suggest that older workers are more flexible in their task choice behavior. Younger workers are more biased towards choosing within‐nest tasks. Finally, there are effects of previous experience that tend to keep ants in familiar tasks. Task allocation based on several mechanisms may balance between: (1) concentrating the most worn workers into the most dangerous tasks; (2) increasing task performance levels; and (3) maintaining behavioral flexibility to respond to demographic perturbations. The degree to which behavior is flexible may correlate to the frequency of such perturbations in a species.