Labor In Social Insects Research Articles

Soldiers in a Stingless Bee.

The differentiation of workers into morphological subcastes (e.g., soldiers) represents an important evolutionary transition and is thought to improve division of labor in social insects. Soldiers occur in many ant and termite species, where they make up a small proportion of the workforce. A common assumption of worker caste evolution is that soldiers are behavioral specialists. Here, we report the first test of the "rare specialist" hypothesis in a eusocial bee. Colonies of the stingless bee Tetragonisca angustula are defended by a small group of morphologically differentiated soldiers. Contrary to the rare specialist hypothesis, we found that soldiers worked more (+34%-41%) and performed a greater variety of tasks (+23%-34%) than other workers, particularly early in life. Our results suggest a "rare elite" function of soldiers in T. angustula, that is, that they perform a disproportionately large amount of the work. Division of labor was based on a combination of temporal and physical castes, but soldiers transitioned faster from one task to the next. We discuss why the rare specialist assumption might not hold in species with a moderate degree of worker differentiation.

Self-organizing techniques to improve the decentralized multi-task distribution in multi-robot systems

This paper focuses on the general problem of coordinating multiple robots, in particular, addresses the problem of the distribution of heterogeneous multi-task in a robust and efficient manner. The main interest in these systems is to understand how from simple rules inspired by the division of labor in social insects, a group of robots can perform tasks in an organized and coordinated way. We take into account a specifically distributed or decentralized approach as we are particularly interested in experimenting with truly autonomous and decentralized techniques in which the robots themselves are responsible for choosing a particular task in an autonomous and individual way. Under this approach we can speak of multi-task selection instead of multi-task assignment, which means, that the agents or robots select the tasks instead of being assigned a task by a central controller. In this regard, we have established an experimental scenario to solve the corresponding multi-task distribution problem and we propose a solution using different approaches by applying the response threshold models inspired by division of labor in social insects, the application of the reinforcement learning algorithm based on learning automata theory and ant colony optimization-based deterministic algorithms. We have evaluated the robustness of the algorithms, perturbing the number of pending loads to simulate the robot׳s error in estimating the real number of pending tasks and also the dynamic generation of loads through time. The paper ends with a critical discussion of experimental results.

Geographic variation in caste ratio of trematode colonies with a division of labour reflect local adaptation.

Similarly to the division of labour in social insects, castes of morphologically distinct individuals exist within colonies of some species of parasitic trematodes. These colonies occur in the first intermediate host of the trematode's complex life cycle and are composed of clonal individuals. Individuals of the reproductive caste have significantly larger bodies while non-reproductive individuals are small and appear to be specialised for defence against co-infecting trematode colonies. In parallel with colony organisation of social insects, demographic traits such as the proportion of the small, non-reproducing individuals relative to the large, reproducing individuals and colony size are expected to vary and adjust to local conditions. In the case of colonies from geographically and potentially genetically distinct populations, this variation is hypothesised to become fixed by evolutionary divergence, as reported in social insect studies. In this study, the adaptive demography theory was further tested by looking at caste ratio and colony organisation of Philophthalmus sp. (a parasitic trematode with a recently discovered division of labour) colonies from geographically distinct populations. Results indicate that the caste ratio from geographically distinct Philophthalmus sp. colonies differs; the proportion of small, defensive individuals is higher in colonies from the location where the risk of competition is highest. This is suggestive of local adaptation, as caste ratios do not change over time under standardised laboratory conditions. This is the first evidence to support the adaptive demography theory in a species with a division of labour other than social insects.

High social density increases foraging and scouting rates and induces polydomy in Temnothorax ants

Many organisms live in crowded groups where social density affects behavior and fitness. Social insects inhabit nests that contain many individuals where physical interactions facilitate information flow and organize collective behaviors such as foraging, colony defense, and nest emigration. Changes in nest space and intranidal crowding can alter social interactions and affect worker behavior. Here, I examined the effects of social density on foraging, scouting, and polydomy behavior in ant colonies—using the species Temnothorax rugatulus. First, I analyzed field colonies and determined that nest area scaled isometrically with colony mass—this indicates that nest area changes proportionally with colony size and suggests that ants actively control intranidal density. Second, laboratory experiments showed that colonies maintained under crowded conditions had greater foraging and scouting activities compared to the same colonies maintained at a lower density. Moreover, crowded colonies were significantly more likely to become polydomous. Polydomous colonies divided evenly based on mass between two nests but distributed fewer, heavier workers and brood to the new nests. Polydomous colonies also showed different foraging and scouting rates compared to the same colonies under monodomous conditions. Combined, the results indicate that social density is an important colony phenotype that affects individual and collective behavior in ants. I discuss the function of social density in affecting communication and the organization of labor in social insects and hypothesize that the collective management of social density is a group level adaptation in social insects.

Sucrose responsiveness, learning success, and task specialization in ants

Social insects possess remarkable learning capabilities, which are crucial for their ecological success. They also exhibit interindividual differences in responsiveness to environmental stimuli, which underlie task specialization and division of labor. Here we investigated for the first time the relationships between sucrose responsiveness, behavioral specialization, and appetitive olfactory learning in ants, including reproductive castes. We show that castes of the ant Camponotus aethiops differ in their responsiveness to sucrose and in their learning success in olfactory conditioning experiments in which sucrose is used as reward. Olfactory learning was better in foragers than in nurses, in agreement with their higher sucrose responsiveness. Interindividual variation in stimulus responsiveness and in learning may be, therefore, a crucial factor for division of labor in social insects.

Genetic polyethism in the polyandrous desert ant Cataglyphis cursor

Several genetic and nongenetic hypotheses have been formulated to account for the evolution and maintenance of multiple mating by females (polyandry) in social Hymenoptera. A major hypothesis argues that polyandry allows production of genetically diverse workers varying in their inclination to perform different tasks, thereby enhancing division of labor and colony task efficiency. We tested the relationship between patriline, worker size, and task specialization in the ant Cataglyphis cursor , a species showing natural variation in queen mating frequency. Our results reveal a significant association between patriline and task preference: workers belonging to different patrilines differ in their propensity to perform a given task (foraging, nest construction, waste management, or food storage). Furthermore, we found that worker size is closely associated with task specialization but not with paternal origin. Overall, these results show that task performance is at least partly genetically influenced in the ant C. cursor , which is a key prerequisite for polyandry to improve division of labor in social insects.

Size‐related variation in protein abundance in the brain and abdominal tissue of bumble bee workers

Female bumble bee workers of the same species often show a profound body size variation that is linked to a division of labour. Large individuals are more likely to forage whereas small individuals are more likely to perform in-nest activities. A higher sensory sensitivity, stronger circadian rhythms as well as better learning and memory performances appear to better equip large individuals for outdoor activities compared to their smaller siblings. The molecular mechanisms underlying worker functional polymorphism remain unclear. Proteins are major determinants of an individual's morphology and behaviour. We hypothesized that the abundance of proteins such as metabolic enzymes as well as proteins involved in neuronal functions would differ with body size and provide insights into the mechanisms underlying size-dependent physiological specialization in bumble bee workers. We conducted protein quantification measurements based on liquid chromatography coupled with tandem mass spectrometry on tissue samples derived from small and large Bombus impatiens and Bombus terrestris workers. Proteins found to differ significantly in abundance between small and large workers belong to the categories of structure, energy metabolism and stress response. These findings provide the first proteomic insight into mechanisms associated with size-based division of labour in social insects.

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 materialThe online version of this article (doi:10.1007/s00265-012-1343-2) contains supplementary material, which is available to authorized users.

Mixing of Honeybees with Different Genotypes Affects Individual Worker Behavior and Transcription of Genes in the Neuronal Substrate

Division of labor in social insects has made the evolution of collective traits possible that cannot be achieved by individuals alone. Differences in behavioral responses produce variation in engagement in behavioral tasks, which as a consequence, generates a division of labor. We still have little understanding of the genetic components influencing these behaviors, although several candidate genomic regions and genes influencing individual behavior have been identified. Here, we report that mixing of worker honeybees with different genotypes influences the expression of individual worker behaviors and the transcription of genes in the neuronal substrate. These indirect genetic effects arise in a colony because numerous interactions between workers produce interacting phenotypes and genotypes across organisms. We studied hygienic behavior of honeybee workers, which involves the cleaning of diseased brood cells in the colony. We mixed ∼500 newly emerged honeybee workers with genotypes of preferred Low (L) and High (H) hygienic behaviors. The L/H genotypic mixing affected the behavioral engagement of L worker bees in a hygienic task, the cooperation among workers in uncapping single brood cells, and switching between hygienic tasks. We found no evidence that recruiting and task-related stimuli are the primary source of the indirect genetic effects on behavior. We suggested that behavioral responsiveness of L bees was affected by genotypic mixing and found evidence for changes in the brain in terms of 943 differently expressed genes. The functional categories of cell adhesion, cellular component organization, anatomical structure development, protein localization, developmental growth and cell morphogenesis were overrepresented in this set of 943 genes, suggesting that indirect genetic effects can play a role in modulating and modifying the neuronal substrate. Our results suggest that genotypes of social partners affect the behavioral responsiveness and the neuronal substrate of individual workers, indicating a complex genetic architecture underlying the expression of behavior.

An Evolutionary Perspective on Self-Organized Division of Labor in Social Insects

Division of labor is a complex phenomenon observed throughout nature. Theoretical studies have focused either on its emergence through self-organization mechanisms or on its adaptive consequences. We suggest that the interaction of self-organization, which undoubtedly characterizes division of labor in social insects, and evolution should be further explored. We review the factors empirically shown to influence task choice. In light of these factors, we review the most important self-organization and evolutionary models for division of labor and outline their advantages and limitations. We describe ways to unify evolution and self-organization in the theoretical study of division of labor and recent results in this area. Finally, we discuss some benchmarks and primary challenges of this approach.

The effect of load on agent-based algorithms for distributed task allocation

Multi-agent algorithms inspired by the division of labour in social insects and by markets, are applied to a constrained problem of distributed task allocation. The efficiency (average number of tasks performed), the flexibility (ability to react to changes in the environment), and the sensitivity to load (ability to cope with differing demands) are investigated in both static and dynamic environments. A hybrid algorithm combining both approaches, is shown to exhibit improved efficiency and robustness. We employ nature inspired particle swarm optimisation to obtain optimised parameters for all algorithms in a range of representative environments. Although results are obtained for large population sizes to avoid finite size effects, the influence of population size on the performance is also analysed. From a theoretical point of view, we analyse the causes of efficiency loss, derive theoretical upper bounds for the efficiency, and compare these with the experimental results.

Teamwork in Self-Organized Robot Colonies

Swarm robotics draws inspiration from decentralized self-organizing biological systems in general and from the collective behavior of social insects in particular. In social insect colonies, many tasks are performed by higher order group or team entities, whose task-solving capacities transcend those of the individual participants. In this paper, we investigate the emergence of such higher order entities. We report on an experimental study in which a team of physical robots performs a foraging task. The robots are "identical" in hardware and control. They make little use of memory and take actions purely on the basis of local information. Our study advances the current state of the art in swarm robotics with respect to the number of real-world robots engaging in teamwork (up to 12 robots in the most challenging experiment). To the best of our knowledge, in this paper we present the first self-organized system of robots that displays a dynamical hierarchy of teamwork (with cooperation also occurring among higher order entities). Our study shows that teamwork requires neither individual recognition nor differences between individuals. This result might also contribute to the ongoing debate on the role of these characteristics in the division of labor in social insects.

Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis

Reproductive division of labor in social insects is accompanied by the reliable communication of individual fertility status. A central question is whether there exists a general mechanism underlying this communication system across species. The best way to produce reliable information is through physiological markers tightly associated with reproductive status. Cuticular hydrocarbons exhibit this link to individual fertility in several species of ants, bees, and wasps, and we present the first evidence for such a system in a non-Hymenopteran eusocial species. In the termite Zootermopsis nevadensis, we identified four polyunsaturated alkenes, which only occur in significant amounts on reproductives that are actively producing gametes. These compounds are either absent or only occur in small amounts in soldiers, worker-like larvae, and secondary reproductives with inactive gonads. In contrast to Hymenopteran social insects, both sexes express the reproductive peaks. The reproductive-specific hydrocarbons may promote tending behavior by worker-like larvae or act as a primer pheromone, inhibiting the reproductive development of immature conspecifics.

Behavioral evolution in the major worker subcaste of twig-nesting Pheidole (Hymenoptera: Formicidae): does morphological specialization influence task plasticity?

Polymorphism frequently correlates with specialized labor in social insects, but extreme morphologies may compromise behavioral flexibility and thus limit caste evolution. The ant genus Pheidole has dimorphic worker subcastes in which major workers appear limited due to their morphology to performing defensive or trophic functions, thus providing an ideal model to investigate specialization and plasticity. We examined worker morphology, brood-care flexibility, and subcaste ratio in 17 species of tropical twig-nesting Pheidole by quantifying nursing by major workers in natural colonies and in subcolonies lacking minors, in which we also measured brood survival and growth. Across species, majors performed significantly less brood care than minors in intact colonies, but increased rates of brood care 20-fold in subcolonies lacking minors. Brood nursed by majors had lower survival than brood tended by minors, although rates of brood growth did not vary between subcastes. Significant interspecific variation in rates of brood care by major workers did not lead to significant differences in brood growth or survival. Additionally, we did not find a significant association between the degree of major worker morphometric specialization and rates of nursing, growth, or survival of brood among species. Therefore, major workers showed reduced efficacy of brood care, but the degree of morphological specialization among species did not directly compromise task plasticity. The compact nests and all-or-nothing consequences of predation or disturbance on colony fitness may have influenced the evolution of major worker brood-care competency in twig-nesting Pheidole.

ADAPTING TO DYNAMIC ENVIRONMENTS: POLYETHISM IN RESPONSE THRESHOLD MODELS FOR SOCIAL INSECTS

Response threshold models are an important tool to model division of labor in social insects and to investigate the underlying principles of self-organization. In this article response threshold models which incorporate dynamic environments with varying demand for work and their influence on division of labor are studied. In their natural habitats, social insects are always exposed to dynamic environments, however, the effect that such environments have on response threshold models has rarely been investigated. In the course of this article it is shown that overworking and underworking, i.e. working more or less than the ideal amount, over a certain time is a colony-size dependent effect in dynamic situations. By adjusting the number of possible learning steps, which correspond to changes in the maximal threshold values relative to a colony's size, the performance of colonies in dynamic environments can be increased. A setup inspired by repeated migration behavior is also investigated. It is shown that these different learning rates affect a colony's ability to maintain an activity onset for a reappearing task.

PDK1 and HR46 Gene Homologs Tie Social Behavior to Ovary Signals

The genetic basis of division of labor in social insects is a central question in evolutionary and behavioral biology. The honey bee is a model for studying evolutionary behavioral genetics because of its well characterized age-correlated division of labor. After an initial period of within-nest tasks, 2–3 week-old worker bees begin foraging outside the nest. Individuals often specialize by biasing their foraging efforts toward collecting pollen or nectar. Efforts to explain the origins of foraging specialization suggest that division of labor between nectar and pollen foraging specialists is influenced by genes with effects on reproductive physiology. Quantitative trait loci (QTL) mapping of foraging behavior also reveals candidate genes for reproductive traits. Here, we address the linkage of reproductive anatomy to behavior, using backcross QTL analysis, behavioral and anatomical phenotyping, candidate gene expression studies, and backcross confirmation of gene-to-anatomical trait associations. Our data show for the first time that the activity of two positional candidate genes for behavior, PDK1 and HR46, have direct genetic relationships to ovary size, a central reproductive trait that correlates with the nectar and pollen foraging bias of workers. These findings implicate two genes that were not known previously to influence complex social behavior. Also, they outline how selection may have acted on gene networks that affect reproductive resource allocation and behavior to facilitate the evolution of social foraging in honey bees.

Reappraising Social Insect Behavior through Aversive Responsiveness and Learning

BackgroundThe success of social insects can be in part attributed to their division of labor, which has been explained by a response threshold model. This model posits that individuals differ in their response thresholds to task-associated stimuli, so that individuals with lower thresholds specialize in this task. This model is at odds with findings on honeybee behavior as nectar and pollen foragers exhibit different responsiveness to sucrose, with nectar foragers having higher response thresholds to sucrose concentration. Moreover, it has been suggested that sucrose responsiveness correlates with responsiveness to most if not all other stimuli. If this is the case, explaining task specialization and the origins of division of labor on the basis of differences in response thresholds is difficult.MethodologyTo compare responsiveness to stimuli presenting clear-cut differences in hedonic value and behavioral contexts, we measured appetitive and aversive responsiveness in the same bees in the laboratory. We quantified proboscis extension responses to increasing sucrose concentrations and sting extension responses to electric shocks of increasing voltage. We analyzed the relationship between aversive responsiveness and aversive olfactory conditioning of the sting extension reflex, and determined how this relationship relates to division of labor.Principal FindingsSucrose and shock responsiveness measured in the same bees did not correlate, thus suggesting that they correspond to independent behavioral syndromes, a foraging and a defensive one. Bees which were more responsive to shock learned and memorized better aversive associations. Finally, guards were less responsive than nectar foragers to electric shocks, exhibiting higher tolerance to low voltage shocks. Consequently, foragers, which are more sensitive, were the ones learning and memorizing better in aversive conditioning.ConclusionsOur results constitute the first integrative study on how aversive responsiveness affects learning, memory and social organization in honeybees. We suggest that parallel behavioral modules (e.g. appetitive, aversive) coexist within each individual bee and determine its tendency to adopt a given task. This conclusion, which is at odds with a simple threshold model, should open new opportunities for exploring the division of labor in social insects.

Specialization Does Not Predict Individual Efficiency in an Ant

The ecological success of social insects is often attributed to an increase in efficiency achieved through division of labor between workers in a colony. Much research has therefore focused on the mechanism by which a division of labor is implemented, i.e., on how tasks are allocated to workers. However, the important assumption that specialists are indeed more efficient at their work than generalist individuals—the “Jack-of-all-trades is master of none” hypothesis—has rarely been tested. Here, I quantify worker efficiency, measured as work completed per time, in four different tasks in the ant Temnothorax albipennis: honey and protein foraging, collection of nest-building material, and brood transports in a colony emigration. I show that individual efficiency is not predicted by how specialized workers were on the respective task. Worker efficiency is also not consistently predicted by that worker's overall activity or delay to begin the task. Even when only the worker's rank relative to nestmates in the same colony was used, specialization did not predict efficiency in three out of the four tasks, and more specialized workers actually performed worse than others in the fourth task (collection of sand grains). I also show that the above relationships, as well as median individual efficiency, do not change with colony size. My results demonstrate that in an ant species without morphologically differentiated worker castes, workers may nevertheless differ in their ability to perform different tasks. Surprisingly, this variation is not utilized by the colony—worker allocation to tasks is unrelated to their ability to perform them. What, then, are the adaptive benefits of behavioral specialization, and why do workers choose tasks without regard for whether they can perform them well? We are still far from an understanding of the adaptive benefits of division of labor in social insects.

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.

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.