Labor In Insect Societies Research Articles

Ontogeny of superorganisms: Social control of queen specialization in ants

Abstract The functioning of biological systems relies on the cooperation of specialized components and understanding the processes that produce such specialization is a major challenge in biology. Here, we study the ontogeny of biological systems at a new phenotypic level: the superorganisms (i.e. insect societies with specialized individuals). We investigate how founding queens, the earliest developmental stage of ant colonies, transition from expressing behavioural pluripotency to becoming strictly specialized in egg production. We demonstrate that the presence of workers both initiates and maintains this queen specialization, and propose that such a social control of queen behaviour is common in ants and regulated by ancestral mechanisms. These findings contradict the traditional view of social insect queens as being intrinsically specialized in egg production and may reshape our understanding of the division of labour in insect societies. Read the free Plain Language Summary for this article on the Journal blog.

Dufour\u2019s gland analysis reveals caste and physiology specific signals in Bombus impatiens

Reproductive division of labor in insect societies is regulated through multiple concurrent mechanisms, primarily chemical and behavioral. Here, we examined if the Dufour’s gland secretion in the primitively eusocial bumble bee Bombus impatiens signals information about caste, social condition, and reproductive status. We chemically analyzed Dufour’s gland contents across castes, age groups, social and reproductive conditions, and examined worker behavioral and antennal responses to gland extracts. We found that workers and queens each possess caste-specific compounds in their Dufour’s glands. Queens and gynes differed from workers based on the presence of diterpene compounds which were absent in workers, whereas four esters were exclusive to workers. These esters, as well as the total amounts of hydrocarbons in the gland, provided a separation between castes and also between fertile and sterile workers. Olfactometer bioassays demonstrated attraction of workers to Dufour’s gland extracts that did not represent a reproductive conflict, while electroantennogram recordings showed higher overall antennal sensitivity in queenless workers. Our results demonstrate that compounds in the Dufour’s gland act as caste- and physiology-specific signals and are used by workers to discriminate between workers of different social and reproductive status.

Scaling relationships in Formica ants with continuous worker size variation

Social insects exhibit highly variable body plans at multiple scales: within colonies, between conspecific colonies, and across different species. The interspecific variation in the existence and prevalence of morphologically discrete worker subcastes in social insects raises questions about the ontogeny and functional importance of alternative worker body plans. Here, we examine the allometry of four Formica species. Formica are among the most common ants in the northern hemisphere temperate zone, and species vary greatly in the degree of worker size variation. However, no Formica species exhibit obvious worker subcastes. By carefully measuring head width, head height, scape length, thorax length, hind femur length, and hind tibia length in 180 individuals, we confirm that Formica workers exhibit continuous linear scaling, meaning that they lack discrete morphological subcastes. Most measurements scale allometrically. Different colonies of the same species are generally consistent in the slope of these relationships, and we detect unexpected similarities in scaling relationships among the four Formica species as well. Some scaling relationships, including a proportionally shorter scape and larger head in large-bodied workers, were also previously found in fire ants. Identifying worker size and shape distributions among different species is a vital step in understanding the selection pressures shaping division of labor in insect societies.

Cross-activity of honeybee queen mandibular pheromone in bumblebees provides evidence for sensory exploitation

AbstractThe evolutionary origin of queen pheromones (QPs), which regulate reproductive division of labor in insect societies, has been explained by two evolutionary scenarios: the sender-precursor hypothesis and the sensory exploitation hypothesis. These scenarios differ in terms of whether the signaling system was built on preadaptations on the part of either the sender queens or the receiver workers. While some social insect QPs—such as cuticular hydrocarbons—were likely derived from ancestral fertility cues and evolved according to the former theory, the honeybee’s queen mandibular pheromone (QMP) has been suggested to act directly on preexisting gene-regulatory networks linked with reproduction. This is evidenced by the fact that QMP has been shown to also inhibit ovary activation in fruit flies, thereby implying exploitation of conserved physiological pathways. To verify whether QMP has similar effects on more closely related eusocial species, we here tested for QMP cross-activity in the bumblebee Bombus terrestris. Interestingly, we found that the non-native QMP blend significantly inhibited egg laying in both worker and queen bumblebees and caused accompanying shifts in ovary activation. The native bumblebee QP pentacosane, by contrast, only inhibited the reproduction of the workers. Overall, these findings support the hypothesis that honeybee QMP likely evolved via a route of sensory exploitation. We argue that such exploitation could allow social insect queens to produce compounds that manipulate the workers to remain sterile, but that a major hurdle would be that the queens themselves would have to be immune to such compounds.

Honeybees possess a structurally diverse and functionally redundant set of queen pheromones.

Queen pheromones, which signal the presence of a fertile queen and induce workers to remain sterile, play a key role in regulating reproductive division of labour in insect societies. In the honeybee, volatiles produced by the queen's mandibular glands have been argued to act as the primary sterility-inducing pheromones. This contrasts with evidence from other groups of social insects, where specific queen-characteristic hydrocarbons present on the cuticle act as conserved queen signals. This led us to hypothesize that honeybee queens might also employ cuticular pheromones to stop workers from reproducing. Here, we support this hypothesis with the results of bioassays with synthetic blends of queen-characteristic alkenes, esters and carboxylic acids. We show that all these compound classes suppress worker ovary development, and that one of the blends of esters that we used was as effective as the queen mandibular pheromone (QMP) mix. Furthermore, we demonstrate that the two main QMP compounds 9-ODA and 9-HDA tested individually were as effective as the blend of all four major QMP compounds, suggesting considerable signal redundancy. Possible adaptive reasons for the observed complexity of the honeybee queen signal mix are discussed.

Effect of temperature and social environment on worker size in the ant Temnothorax nylanderi

Warm temperatures decrease insect developmental time and body size. Social life could buffer external environmental variations, especially in large social groups, either through behavioral regulation and compensation or through specific nest architecture. Mean worker size and distribution of worker sizes within colonies are important parameters affecting colony productivity as worker size is linked to division of labor in insect societies. In this paper, we investigate the effect of stressful warm temperatures and the role of social environment (colony size and size of nestmate workers) on the mean size and size variation of laboratory-born workers in the small European ant Temnothorax nylanderi. To do so, we reared field-collected colonies under medium or warm temperature treatments after having marked the field-born workers and removed the brood except for 30 first instar larvae. Warm temperature resulted in the production of fewer workers and a higher adult mortality, confirming that this regime was stressful for the ants. T. nylanderi ants followed the temperature size rule observed in insects, with a decreased developmental time and mean size under warm condition. Social environment appeared to play an important role as we observed that (i) larger colonies buffered the effect of temperature better than smaller ones (ii) colonies with larger workers produced larger workers whatever the rearing temperature and (iii) the coefficient of variation of worker size was similar in the field and under medium laboratory temperature. This suggests that worker size variation is not primarily due to seasonal environmental fluctuations in the field. Finally, we observed a higher coefficient of variation of worker size under warm temperature. We propose that this results from a disruption of social regulation, i.e. the control of nestmate workers over developing larvae and adult worker size, under stressful conditions.

Repeated evolution of soldier sub-castes suggests parasitism drives social complexity in stingless bees

The differentiation of workers into morphological castes represents an important evolutionary innovation that is thought to improve division of labor in insect societies. Given the potential benefits of task-related worker differentiation, it is puzzling that physical worker castes, such as soldiers, are extremely rare in social bees and absent in wasps. Following the recent discovery of soldiers in a stingless bee, we studied the occurrence of worker differentiation in 28 stingless bee species from Brazil and found that several species have specialized soldiers for colony defence. Our results reveal that worker differentiation evolved repeatedly during the last ~ 25 million years and coincided with the emergence of parasitic robber bees, a major threat to many stingless bee species. Furthermore, our data suggest that these robbers are a driving force behind the evolution of worker differentiation as targets of robber bees are four times more likely to have nest guards of increased size than non-targets. These findings reveal unexpected diversity in the social organization of stingless bees.

Ant larvae regulate worker foraging behavior and ovarian activity in a dose-dependent manner.

Division of labor in insect societies relies on simple behavioral rules, whereby individual colony members respond to dynamic signals indicating the need for certain tasks to be performed. This in turn gives rise to colony-level phenotypes. However, empirical studies quantifying colony-level signal-response dynamics are lacking. Here, we make use of the unusual biology and experimental amenability of the queenless clonal raider ant Cerapachys biroi, to jointly quantify the behavioral and physiological responses of workers to a social signal emitted by larvae. Using automated behavioral quantification and oocyte size measurements in colonies of different sizes and with different worker to larvae ratios, we show that the workers in a colony respond to larvae by increasing foraging activity and inhibiting ovarian activation in a progressive manner, and that these responses are stronger in smaller colonies. This work adds to our knowledge of the processes that link plastic individual behavioral/physiological responses to colony-level phenotypes in social insect colonies.

Worker self-restraint and policing maintain the queen’s reproductive monopoly in a pseudomyrmecine ant

Division of reproductive labor in insect societies is often based on worker self-restraint and both queen and worker policing. Workers of many hitherto studied wasps, bees and ants do not lay eggs in the presence of a queen. However, it is presently unclear how far these observations in a few select clades can be generalized. We investigated if and how queens maintain a reproductive monopoly in colonies of the elongate twig ant, Pseudomyrmex gracilis, a member of the previously unstudied ant subfamily Pseudomyrmecinae. Colonies are usually headed by a single, singly mated queen (monogyny, monandry). Workers therefore would be more closely related to males produced by other workers (r = 0.375) than to the sons of queens (r = 0.25). Nevertheless, workers appear to refrain from laying male-destined eggs in the presence of the queen. In queenless conditions, workers form dominance hierarchies by antennal boxing, and only one or a few high-ranking individuals readily begin to lay eggs. When returned into a queenright colony, egg-laying workers are immediately bitten, stung and expelled or killed by other workers. While the composition of cuticular hydrocarbons clearly differed between castes, it less clearly reflected worker ovarian development. An association with worker ovarian development that would allow workers to monitor the reproductive status of nestmates could only be tentatively postulated for certain substances. Our study broadens our knowledge about reproductive conflict in social Hymenoptera and shows that worker sterility in the presence of a queen is more common in monogynous, monandrous ants than expected from relatedness alone.

Models of Division of Labor in Insect Societies

Models of Division of Labor in Insect Societies

GENETIC COMPATIBILITY AFFECTS DIVISION OF LABOR IN THE ARGENTINE ANTLINEPITHEMA HUMILE

Division of labor is central to the organization of insect societies. Within-colony comparisons between subfamilies of workers (patrilines or matrilines) revealed genetic effects on division of labor in many social insect species. Although this has been taken as evidence for additive genetic effects on division of labor, it has never been experimentally tested. To determine the relative roles of additive and nonadditive genetic effects (e.g., genetic compatibility, epistasis, and parent-of-origin imprinting effects) on worker behavior, we performed controlled crosses using the Argentine ant Linepithema humile. Three of the measured behaviors (the efficiency to collect pupae, the foraging propensity, and the distance between non-brood-tenders and brood) were affected by the maternal genetic background and the two others (the efficiency to feed larvae and the distance between brood-tenders and brood) by the paternal genetic background. Moreover, there were significant interactions between the maternal and paternal genetic backgrounds for three of the five behaviors. These results are most consistent with parent-of-origin and genetic compatibility effects on division of labor. The finding of nonadditive genetic effects is in strong contrast with the current view and has important consequences for our understanding of division of labor in insect societies.

Research on Improved Division of Labor in Ant Colonies for Task Allocations

In nature there exist many mechanisms giving rise to self-regulation. One such mechanism is the division of labor in insect societies. However, it may be simple and difficult to be applied in practice. Due to these reasons, an improved model of labor division is proposed considering multi-states and capability constraints of ant individual. At last, two simulation experiments, where one is a task allocation problem of agile manufacturing mode corresponding to a basic mathematical model for labor division and the other is a logistic distribution problem corresponding to an improved mathematical model, are given so as to verify its efficiency and effectiveness and some meaningful results are obtained.

Social Evolution of Spatial Patterns in Bacterial Biofilms: When Conflict Drives Disorder

A key feature of biological systems is the emergence of higher-order structures from interacting units, such as the development of tissues from individual cells and the elaborate divisions of labor in insect societies. Little is known, however, of how evolutionary competition among individuals affects biological organization. Here we explore this link in bacterial biofilms, concrete systems that are well known for higher-order structures. We present a mechanistic model of cell growth at a surface, and we show that tension between growth and competition for nutrients can explain how empirically observed patterns emerge in biofilms. We then apply our model to evolutionary simulations and observe that the maintenance of patterns requires cooperation between cells. Specifically, when different genotypes meet and compete, natural selection favors energetically costly spreading strategies, like polymer secretion, that simultaneously reduce productivity and disrupt the spatial patterns. Our theory provides a formal link between higher-level patterning and the potential for evolutionary conflict by showing that both can arise from a single set of scale-dependent processes. Moreover, and contrary to previous theory, our analysis predicts an antagonistic relationship between evolutionary conflict and pattern formation: conflict drives disorder.

Division of labour in ant colonies in terms of attractive fields

In nature there exist many mechanisms giving rise to self-regulation. One such mechanism is the division of labour in insect societies. Within this work we propose a mathematical model for the allocation of tasks in ant colonies, where each of the tasks is represented by an attractive field. This can be seen as a stimulus, whose strength is inversely proportional to the distance to the task. The dynamics leading to the division of labour is therefore driven by the spatial distance of the ants to the source of information encoding the task. Assuming homogeneity among the ants, specialisation and adaptability are obtained through the introduction of learning and forgetting.

Genetic and genomic analyses of the division of labour in insect societies

Division of labour--individuals specializing in different activities--features prominently in the spectacular success of the social insects. Until recently, genetic and genomic analyses of division of labour were limited to just a few species. However, research on an ever-increasing number of species has provided new insight, from which we highlight two results. First, heritable influences on division of labour are more pervasive than previously imagined. Second, different forms of division of labour, in lineages in which eusociality has arisen independently, have evolved through changes in the regulation of highly conserved molecular pathways associated with several basic life-history traits, including nutrition, metabolism and reproduction.

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.

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.

Bio-inspired scheduling for dynamic job shops with flexible routing and sequence-dependent setups

Flexible routing requires scheduling to be responsive and robust. Multi-agent systems have the potential to achieve robustness and provide a means for real-time planning and scheduling. The objective of this paper is to propose a multi-agent scheduling system with a good solution quality and robustness. The proposed multi-agent approach is designed for dynamic job shops with routing flexibility and sequence-dependent setup. A bio-inspired strategy based on division of labour in insect societies is presented for coordination among agents. The strategy is accomplished using a computational model which is composed of response threshold, response intention, and machine-centred reinforcement learning. The bio-inspired scheduling is compared with an agent-based approach and a dispatching rule-based approach. The experiments were performed using simulation and statistical analysis. Results show that the proposed bio-inspired scheduling model performs better than the other two methods on all eight common scheduling metrics.

Environment- and Age-Dependent Plasticity of Synaptic Complexes in the Mushroom Bodies of Honeybee Queens

Diversity in behavior plays a crucial role for the division of labor in insect societies. Social insects such as honeybees provide excellent model systems to investigate neuronal principles underlying behavioral plasticity. The two female castes, queens and workers, differ substantially in anatomy, physiology, aging and behavior. The different phenotypes are induced by environmental factors rather than genetic differences. Here we investigated environment- and age-dependent effects on the synaptic organization within higher order neuropils of the honeybee brain. Synaptic complexes (microglomeruli) in sensory-input regions of the mushroom bodies, prominent higher sensory integration centers, were analyzed quantitatively using fluorescent markers and confocal microscopy. Pre- and postsynaptic compartments of individual microglomeruli were labeled by anti-synapsin immunolabeling and f-actin detection with phalloidin in dendritic spines of mushroom-body intrinsic neurons. The results demonstrate that in queens the numbers of microglomeruli in the olfactory and visual input regions of the mushroom-body calyx are significantly lower than in workers. In queens raised in incubators, microglomeruli were affected by differences in pupal rearing temperature within the range of naturally occurring temperatures (32–36°C). The highest numbers of microglomeruli developed at a lower temperature compared to workers (33.5 vs. 34.5°C). We found a striking adult plasticity of microglomeruli numbers throughout the extended life-span of queens. Whereas microglomeruli in the olfactory lip increased with age (∼55%), microglomeruli in the visual collar significantly decreased (∼35%). We propose that developmental and adult plasticity of the synaptic circuitry in the mushroom-body calyx might underlie caste- and age-specific adaptations in behavior.

Polybia wasp biting interactions recruit foragers following experimental worker removals

Communicative interactions between colony members, or worker connectivity, can affect division of labour in insect societies. Nestmate workers of the eusocial paper wasp Polybia occidentalis engage in biting interactions, and correlational evidence suggests that biting promotes foraging by the workers that are bitten. I used experimental forager removals to test whether biting is a form of worker connectivity, inducing new recruits to enter the foraging force. I observed colonies with marked workers during a pretreatment (control) period, then removed all arriving foragers on the following day. Foraging ceased after several hours of forager removals, and remained depressed on the following morning. I grouped the remaining workers into four behavioural categories: nonforagers, individuals that stopped foraging after the manipulation, continuing foragers that were active before and after the manipulation and recruited foragers that began foraging after the manipulation. After the manipulation, the recruited foragers were bitten at similar rates to the continuing foragers and, most importantly, were the only ones that were bitten at significantly increased rates after the manipulation. Most recruits were observed being bitten before they began foraging. However, some recruits were not observed being bitten, and worker responses to biting were often gradual. These patterns suggest that the effect of biting is to modulate the probability of foraging in bitten workers. The experiments show that biting helps to induce foraging. Biting is a form of worker connectivity, serving as a mechanism of communication between Polybia workers that affects colony responses to changing conditions.