Labor In Social Insects Research Articles

Ant social network structure is highly conserved across species.

The ecological success of social insects makes their colony organization fascinating to scientists studying collective systems. In recent years, the combination of automated behavioural tracking and social network analysis has deepened our understanding of many aspects of colony organization. However, because studies have typically worked with single species, we know little about interspecific variation in network structure. Here, we conduct a comparative network analysis across five ant species from five subfamilies, separated by more than 100 Myr of evolution. We find that social network structure is highly conserved across subfamilies. All species studied form modular networks, with two social communities, a similar distribution of individuals between the two communities, and equivalent mapping of task performance onto the communities. Against this backdrop of organizational similarity, queens of the different species occupied qualitatively distinct network positions. The deep conservation of the two community structure implies that the most fundamental behavioural division of labour in social insects is between workers that stay in the nest to rear brood, and those that leave the nest to forage. This division has parallels across the animal kingdom in systems of biparental care and probably represents the most readily evolvable form of behavioural division of labour.

Effect of Juvenile Hormone on Worker Behavioral Transition in the Red Imported Fire Ant, Solenopsis invicta (Hymenoptera: Formicidae).

The division of labor among workers is a defining characteristic of social insects and plays a pivotal role in enhancing the competitive advantage of their colony. Juvenile hormone (JH) has long been hypothesized to be the essential driver in regulating the division of labor due to its ability to accelerate behavioral transitions in social insects, such as honeybees. The regulation of behavioral transitions by JH in the red imported fire ant (RIFA), Solenopsis invicta, a typical social pest, is unclear. Through video capture and analysis, we investigated the effects of the juvenile hormone analogue (JHA) methoprene on brood care, phototaxis behavior, and threat responsiveness of RIFA nurse workers. Our results showed that the JHA application significantly reduced the time and frequency of brood care behavior by nurse workers while increasing their walking distance and activity time in the light area. Additionally, the application of JHA made ants become excited, indicating a significant improvement in their activity level (movement distance, time, and speed). Furthermore, it was observed that the application of JHA did not affect the threat responsiveness of nurse workers towards stimuli (nestmates or non-nestmates). Our study demonstrates that the application of JHA reduced brood care behavior and enhanced phototaxis in nurse workers, which may reveal the role of JH in facilitating behavioral transitions in RIFA from intranidal tasks to extranidal activity. This study provides an experimental basis for further elucidating the mechanism underlying the division of labor in social insects.

Maintenance mechanisms of the division of labor in social insects

アリやミツバチ，シロアリなどの真社会性昆虫は，コロニーメンバー間の分業を特徴として，様々な環境下において生態学的成功を実現している。コロニーは生殖を担う生殖個体と，それ以外のすべての作業を行う非繁殖の労働個体（ワーカー）による２つのサブグループで構成されている。 さらに，ワーカーの間でも労働に関する分業が生じており，ワーカーはコロニー内で異なる仕事に従事している。ワーカー間の労働分業は社会進化と密接に関係しており，分業の維持機構は個体レベルからコロニーレベルまで幅広く研究されている分野である。本総説では，労働分業の維持機構に関する最近の研究成果をまとめて紹介する。特に，ワーカーの行動可塑性が集団レベルの表現型としての分業をどのように形成しているかに注目して議論を進める。まず，分業を維持する２つのメカニズム，すなわち齢差分業と柔軟なタスク変更を説明したのち，分業を定量的に評価するための方法を紹介する。次に，ワーカーの意思決定に関わるタスクの反応閾値がどのようにタスクの遂行と関係するのか説明する。次に，分業の生理的基盤について，特に幼若ホルモンとビテロジェニン，ビテロジェニン関連遺伝子に着目して知見をまとめる。また，分業を維持する上で重要な要因となるワーカーのタスク移行のメカニズムについて議論する。最後に，社会性昆虫における分業に関する研究の今後の方向性について述べる。

Social complexity, life-history and lineage influence the molecular basis of castes in vespid wasps

A key mechanistic hypothesis for the evolution of division of labour in social insects is that a shared set of genes co-opted from a common solitary ancestral ground plan (a genetic toolkit for sociality) regulates caste differentiation across levels of social complexity. Using brain transcriptome data from nine species of vespid wasps, we test for overlap in differentially expressed caste genes and use machine learning models to predict castes using different gene sets. We find evidence of a shared genetic toolkit across species representing different levels of social complexity. We also find evidence of additional fine-scale differences in predictive gene sets, functional enrichment and rates of gene evolution that are related to level of social complexity, lineage and of colony founding. These results suggest that the concept of a shared genetic toolkit for sociality may be too simplistic to fully describe the process of the major transition to sociality.

King- and queen-specific degradation of uric acid contributes to reproduction in termites.

Caste-based reproductive division of labour in social insects is built on asymmetries in resource allocation within colonies. Kings and queens dominantly consume limited resources for reproduction, while non-reproductive castes such as workers and soldiers help reproductive castes. Studying the regulation of such asymmetries in resource allocation is crucial for understanding the maintenance of sociality in insects, although the molecular background is poorly understood. We focused on uric acid, which is reserved and used as a valuable nitrogen source in wood-eating termites. We found that king- and queen-specific degradation of uric acid contributes to reproduction in the subterranean termite Reticulitermes speratus. The urate oxidase gene (RsUAOX), which catalyses the first step of nitrogen recycling from stored uric acid, was highly expressed in mature kings and queens, and upregulated with differentiation into neotenic kings/queens. Suppression of uric acid degradation decreased the number of eggs laid per queen. Uric acid was shown to be provided by workers to reproductive castes. Our results suggest that the capacity to use nitrogen, which is essential for the protein synthesis required for reproduction, maintains colony cohesion expressed as the reproductive monopoly held by kings and queens.

Two simple movement mechanisms for spatial division of labour in social insects

Many animal species divide space into a patchwork of home ranges, yet there is little consensus on the mechanisms individuals use to maintain fidelity to particular locations. Theory suggests that animal movement could be based upon simple behavioural rules that use local information such as olfactory deposits, or global strategies, such as long-range biases toward landmarks. However, empirical studies have rarely attempted to distinguish between these mechanisms. Here, we perform individual tracking experiments on four species of social insects, and find that colonies consist of different groups of workers that inhabit separate but partially-overlapping spatial zones. Our trajectory analysis and simulations suggest that worker movement is consistent with two local mechanisms: one in which workers increase movement diffusivity outside their primary zone, and another in which workers modulate turning behaviour when approaching zone boundaries. Parallels with other organisms suggest that local mechanisms might represent a universal method for spatial partitioning in animal populations.

Activities of Antioxidant and Proteolytic Systems and Biomarkers in the Fat Body and Hemolymph of Young Apis mellifera Females.

Simple SummaryThe proteolytic system consists of compounds that, similar to “scissors”, cut proteins found in bee cells (e.g., to activate these proteins) or released by pathogens. During these reactions, reactive oxygen species are created and then removed by antioxidants. The actions of the proteolytic and antioxidant systems are enhanced by biomarkers. These compounds are produced mainly in the fat body and then released into the hemolymph. We determined the activities of these compounds in various localizations/segments of the fat body and in the hemolymph in females with increased reproductive potential, i.e., queens and rebels, and in normal (sterile non-rebel) workers. Rebels are workers who resemble the queen in terms of anatomical, behavioural, and physiological features. It was revealed that the activities of these compounds in the rebels were between those of queens and normal workers. Normal workers had higher activities of the proteolytic and antioxidant systems in the fat body and hemolymph than the other females. These results are important for understanding the functioning of the fat body, the stress ecology, and the formation of the different castes of Apis mellifera females.The proteolytic and antioxidant systems are important components of humoral immunity, and these biomarkers indicate the immune status. These compounds are synthesized in the bees’ fat body and released into the hemolymph. Their functions maintain the organism’s homeostasis and protect it against adverse environmental factors (including pathogens). We determined the activities of acidic, neutral, and alkaline proteases and their inhibitors, as well as superoxide dismutase (SOD), catalase (CAT), aspartate aminotransferase (AST), alanine aminotransferase (ALT), alkaline phosphatase (ALP), and the level of total antioxidant potential (TAC). These compounds were investigated in the fat body and hemolymph in the females with increased reproductive potential, i.e., queens and rebels, and in normal (non-reproductive sterile non-rebel) workers. The phenoloxidase (PO) activities were determined in the hemolymph. The normal workers had higher activities of proteases and their inhibitors, SOD and CAT, in the fat body and hemolymph, compared to the queens and rebels. The protease inhibitors were not usually active in the queens. As we predicted, the rebels revealed values between those of the queens and normal workers. The highest activities of proteases and antioxidants were identified in the fat body from the third tergite in comparison with the sternite and the fifth tergite. These results are important for oxidative stress ecology and give a better understanding of the functioning of the fat body and the division of labor in social insects.

Time-course RNASeq of Camponotus floridanus forager and nurse ant brains indicate links between plasticity in the biological clock and behavioral division of labor

BackgroundCircadian clocks allow organisms to anticipate daily fluctuations in their environment by driving rhythms in physiology and behavior. Inter-organismal differences in daily rhythms, called chronotypes, exist and can shift with age. In ants, age, caste-related behavior and chronotype appear to be linked. Brood-tending nurse ants are usually younger individuals and show “around-the-clock” activity. With age or in the absence of brood, nurses transition into foraging ants that show daily rhythms in activity. Ants can adaptively shift between these behavioral castes and caste-associated chronotypes depending on social context. We investigated how changes in daily gene expression could be contributing to such behavioral plasticity in Camponotus floridanus carpenter ants by combining time-course behavioral assays and RNA-Sequencing of forager and nurse brains.ResultsWe found that nurse brains have three times fewer 24 h oscillating genes than foragers. However, several hundred genes that oscillated every 24 h in forager brains showed robust 8 h oscillations in nurses, including the core clock genes Period and Shaggy. These differentially rhythmic genes consisted of several components of the circadian entrainment and output pathway, including genes said to be involved in regulating insect locomotory behavior. We also found that Vitellogenin, known to regulate division of labor in social insects, showed robust 24 h oscillations in nurse brains but not in foragers. Finally, we found significant overlap between genes differentially expressed between the two ant castes and genes that show ultradian rhythms in daily expression.ConclusionThis study provides a first look at the chronobiological differences in gene expression between forager and nurse ant brains. This endeavor allowed us to identify a putative molecular mechanism underlying plastic timekeeping: several components of the ant circadian clock and its output can seemingly oscillate at different harmonics of the circadian rhythm. We propose that such chronobiological plasticity has evolved to allow for distinct regulatory networks that underlie behavioral castes, while supporting swift caste transitions in response to colony demands. Behavioral division of labor is common among social insects. The links between chronobiological and behavioral plasticity that we found in C. floridanus, thus, likely represent a more general phenomenon that warrants further investigation.

Bumble bee queen pheromones are context-dependent

Queen pheromones have long been studied as a major factor regulating reproductive division of labor in social insects. Hitherto, only a handful of queen pheromones were identified and their effects on workers have mostly been studied in isolation from the social context in which they operate. Our study examined the importance of behavioral and social context for the perception of queen semiochemicals by bumble bee workers. Our results indicate that a mature queen’s cuticular semiochemicals are capable of inhibiting worker reproduction only when accompanied by the queen’s visual presence and the offspring she produces, thus, when presented in realistic context. Queen’s chemistry, queen’s visual presence and presence of offspring all act to regulate worker reproduction, but none of these elements produces an inhibitory effect on its own. Our findings highlight the necessity to reconsider what constitutes a queen pheromone and suggest a new approach to the study of chemical ecology in social insects.

Response thresholds alone cannot explain empirical patterns of division of labor in social insects.

The effects of heterogeneity in group composition remain a major hurdle to our understanding of collective behavior across disciplines. In social insects, division of labor (DOL) is an emergent, colony-level trait thought to depend on colony composition. Theoretically, behavioral response threshold models have most commonly been employed to investigate the impact of heterogeneity on DOL. However, empirical studies that systematically test their predictions are lacking because they require control over colony composition and the ability to monitor individual behavior in groups, both of which are challenging. Here, we employ automated behavioral tracking in 120 colonies of the clonal raider ant with unparalleled control over genetic, morphological, and demographic composition. We find that each of these sources of variation in colony composition generates a distinct pattern of behavioral organization, ranging from the amplification to the dampening of inherent behavioral differences in heterogeneous colonies. Furthermore, larvae modulate interactions between adults, exacerbating the apparent complexity. Models based on threshold variation alone only partially recapitulate these empirical patterns. However, by incorporating the potential for variability in task efficiency among adults and task demand among larvae, we account for all the observed phenomena. Our findings highlight the significance of previously overlooked parameters pertaining to both larvae and workers, allow the formulation of theoretical predictions for increasing colony complexity, and suggest new avenues of empirical study.

Social insects: Stochastic switches and behavioral maturation in ants

Changes in behavior with age are widespread in social insects. Lifetime behavioral tracking of individual ants shows these changes are fast and stereotyped, yet stochastically timed. The finding may help shed light on the mechanisms of behavioral maturation and their role in division of labor in social insects.

Pheromonal Regulation of the Reproductive Division of Labor in Social Insects.

The reproductive altruism in social insects is an evolutionary enigma that has been puzzling scientists starting from Darwin. Unraveling how reproductive skew emerges and maintains is crucial to understand the reproductive altruism involved in the consequent division of labor. The regulation of adult worker reproduction involves conspecific inhibitory signals, which are thought to be chemical signals by numerous studies. Despite the primary identification of few chemical ligands, the action modes of primer pheromones that regulate reproduction and their molecular causes and effects remain challenging. Here, these questions were elucidated by comprehensively reviewing recent advances. The coordination with other modalities of queen pheromones (QPs) and its context-dependent manner to suppress worker reproduction were discussed under the vast variation and plasticity of reproduction during colony development and across taxa. In addition to the effect of QPs, special attention was paid to recent studies revealing the regulatory effect of brood pheromones. Considering the correlation between pheromone and hormone, this study focused on the production and perception of pheromones under the endocrine control and highlighted the pivotal roles of nutrition-related pathways. The novel chemicals and gene pathways discovered by recent works provide new insights into the understanding of social regulation of reproductive division of labor in insects.

A small family business: synergistic and additive effects of the queen and the brood on worker reproduction in a primitively eusocial bee.

The mechanisms that maintain reproductive division of labor in social insects are still incompletely understood. Most studies focus on the relationship between adults, overlooking another important stakeholder - the juveniles. Recent studies show that not only the queen but also the brood regulate worker reproduction. However, how the two coordinate to maintain reproductive monopoly remained unexplored. Here, we disentangled the roles of the brood and the queen in primitively eusocial bees (Bombus impatiens) by examining their separated and combined effects on worker behavioral, physiological and brain gene expression. We found that young larvae produce a releaser effect on workers, decreasing oviposition and aggression, while the queen produces both releaser and primer effects, modifying worker behavior and reproductive physiology. The expression of reproduction- and aggression-related genes was altered in the presence of both queen and brood but was stronger or the same in the presence of the queen. We identified two types of interactions between the queen and the brood in regulating worker reproduction: (1) synergistic interactions regulating worker physiology, where the combined effect of the queen and the brood on worker physiology was greater than their separate effects; (2) additive interactions, where the combined effect of the queen and the brood on worker behavior was similar to the sum of their separate effects. Our results suggest that the queen and the brood interact synergistically and additively to regulate worker behavior and reproduction, and this interaction exists at multiple regulatory levels.

Differential responses to chemical cues correlate with task performance in ant foragers

Division of labor in social insects has been explained by response threshold models which are based on differential responses to task-specific stimuli. In the present study, we argue that other types of stimuli, such as location-related cues, which are correlated with but not directly linked to task performance, may be significant. Using the black garden ant Lasius niger as a model, we focused on three groups of workers that perform extranidal tasks: (1) scouts, which explore new and unmarked areas remote from the nest; (2) patrollers, which are not recruited by other ants, but nonetheless walk outside in the nest vicinity; and (3) recruits, which are temporary foragers whose exit is triggered by recruitment. We used standardized tests to investigate, in a context-independent way, whether differences in task performance by these three groups could be correlated to intrinsic differences in their responsiveness to trail pheromone or to nest-related stimuli such as the presence of nestmates or colony odor. Overall, we found that the task profile of workers was correlated neither with their tendency to explore unmarked areas nor with their social attraction to nestmates. Scouts showed a lower attraction to colony odor and lower scores of trail following than recruits. Conversely, recruits were more attracted to colony chemical cues and showed lower response threshold to trail pheromone. Patrollers displayed behaviors between those of recruits and scouts. Our study thus shows that differences in ant responsiveness to location-related cues and recruitment trails contribute to the regulation of extranidal tasks in ants. Work organization in insect societies has been explained by models of differential response thresholds to stimuli that are directly linked to the performance of specific tasks. However, the task performance of individuals could also depend on their responsiveness to social and location-related cues that are correlated but not directly linked to these tasks. Using standardized context-independent tests, we found that scout ants, which explore unknown areas, display a lower responsiveness to colony area marking and trail pheromone. Conversely, recruits, which forage outside the nest only during food exploitation, are the most attracted to nestmates, colony area marking and trail pheromone. Patrollers display intermediate levels of attraction. Location-related cues could therefore play a role in determining the level of task performance by ants and should be taken into consideration in threshold models of task allocation.

Within-individual behavioural variability and division of labour in social insects.

Division of labour, whereby individuals divide the workload in a group, is a recurrent property of social living. The current conceptual framework for division of labour in social insects is provided by the response-threshold model. This model posits that the differences between individuals (i.e. between-individual variability) in responsiveness to task-associated stimuli is a key feature for task specialisation. The consistency of individual behaviours (i.e. within-individual variability) in task performance represents an additional but little-considered component driving robust patterns of division of labour. On the one hand, the presence of workers with a high level of within-individual variability presumably allows colonies to rapidly adapt to external fluctuations. On the other hand, a reduced degree of within-individual variability promotes a stricter specialisation in task performance, thereby limiting the costs of task switching. The ideal balance between flexibility and canalisation probably varies depending on the developmental stage of the colony to satisfy its changing needs. Here, I introduce the main sources of within-individual variability in behaviours in social insects and I review neural correlates accompanying the changes in behavioural flexibility. I propose the hypothesis that the positive scaling between group size and the intensity of task specialisation, a relationship consistently reported both within and between taxa, may rely on reduced within-individual variability via self-organised processes linked to the quality of brood care. Overall, I emphasise the need for a more comprehensive characterisation of the response dynamics of individuals to better understand the mechanisms shaping division of labour in social insects.

Doublesex Evolution Is Correlated with Social Complexity in Ants.

The Dmrt (doublesex and mab-3-related transcription factor) genes are transcription factors crucial for sex determination and sexual differentiation. In some social insects, doublesex (dsx) exhibits widespread caste-specific expression across different tissues and developmental stages and has been suggested as a candidate gene for regulating division of labor in social insects. We therefore conducted a molecular evolution analysis of the Dmrt gene family in 20 ants. We found that the insect-specific oligomerization domain of DSX, oligomerization domain 2, was absent in all ants, except for the two phylogenetically basal ant species (Ponerinae), whose social structure and organization resemble the presumed ancestral condition in ants. Phylogenetic reconstruction and selection analysis revealed that dsx evolved faster than the other three members of the Dmrt family. We found evidence for positive selection for dsx in the ant subfamilies with more advanced social organization (Myrmicinae and Formicinae), but not in the Ponerinae. Furthermore, we detected expression of two Dmrt genes, dsx and DMRT11E, in adult ants, and found a clear male-biased expression pattern of dsx in most species for which data are available. Interestingly, we did not detect male-biased expression of dsx in the two ant species that possess a genetic caste determination system. These results possibly suggest an association between the evolution of dsx and social organization as well as reproductive division of labor in ants.

Stochastic spatial model for the division of labor in social insects

Motivated by the study of social insects, we introduce a stochastic model based on interacting particle systems in order to understand the effect of communication on the division of labor. Members of the colony are located on the vertex set of a graph representing a communication network. They are characterized by one of two possible tasks, which they update at a rate equal to the cost of the task they are performing by either defecting by switching to the other task or cooperating by anti-imitating a random neighbor in order to balance the amount of energy spent in each task. We prove that, at least when the probability of defection is small, the division of labor is poor when there is no communication, better when the communication network consists of a complete graph, but optimal on bipartite graphs with bipartite sets of equal size, even when both tasks have very different costs. This shows a non-monotonic relationship between the number of connections in the communication network and how well individuals organize themselves to accomplish both tasks equally.

Evaluation of Possible Proximate Mechanisms Underlying the Kinship Theory of Intragenomic Conflict in Social Insects.

Kinship theory provides a universal framework in which to understand the evolution of altruism, but there are many molecular and genetic mechanisms that can generate altruistic behaviors. Interestingly, kinship theory specifically predicts intragenomic conflict between maternally-derived alleles (matrigenes) and paternally-derived alleles (patrigenes) over the generation of altruistic behavior in cases where the interests of the matrigenes and patrigenes are not aligned. Under these conditions, individual differences in selfish versus altruistic behavior are predicted to arise from differential expression of the matrigenes and patrigenes (parent-specific gene expression or PSGE) that regulate selfish versus altruistic behaviors. As one of the leading theories to describe PSGE and genomic imprinting, kinship theory has been used to generate predictions to describe the reproductive division of labor in social insect colonies, which represents an excellent model system to test the hypotheses of kinship theory and examine the underlying mechanisms driving it. Recent studies have confirmed the predicted differences in the influence of matrigenes and patrigenes on reproductive division of labor in social insects, and demonstrated that these differences are associated with differences in PSGE of key genes involved in regulating reproductive physiology, providing further support for kinship theory. However, the mechanisms mediating PSGE in social insects, and how PSGE leads to differences in selfish versus altruistic behavior, remain to be determined. Here, we review the available supporting evidence for three possible epigenetic mechanisms (DNA methylation, piRNAs, and histone modification) that may generate PSGE in social insects, and discuss how these may lead to variation in social behavior.

Colony and evolutionary dynamics of a two‐stage model with brood cannibalism and division of labor in social insects

AbstractDivision of labor (DOL) is a major factor for the great success of social insects because it increases the efficiency of a social group where different individuals perform different tasks repeatedly and presumably with increased performance. Cannibalism plays an important role in regulating colony growth and development by regulating the number of individuals in a colony and increasing survival by providing access to essential nutrients and minimizing competition among colony mates. To understand the synergy effects of DOL and cannibalistic behavior on colony dynamic outcomes, we propose and study a compartmental two‐stage model using ecological and evolutionary game theory settings. Our analytical results of the ecological and evolutionary models suggest that: (1) A noncannibalistic colony can survive if the efficiency of energy investment reflecting the DOL is greater than the relative death rate of the older population. (2) A cannibalistic colony can die out if both the efficiency of energy investment and the relative cannibalism rate (where each is also reflecting the DOL) are too large; or if the relative cannibalism rate alone is too small. (3) From our numerical analysis, cannibalism can increase or reduce the colony's total population size, which greatly depends on the benefit of egg cannibalism increasing or decreasing of adult's lifespan. (4) A cannibalistic and noncannibalistic colony can experience bistability due to cooperative behavior. (5) In the evolutionary settings, DOL can prevent colony death and natural selection can preserve strong Allee effects by selecting the traits with the largest investment on brood care and the lowest cannibalism rate. (6) Evolutionary dynamics may increase the fitness of the colony, i.e., the successful production of workforce which results in the increase of total worker population size, colony survival, and reproduction. Our results suggest both cannibalism and DOLs are adaptive strategies that increase the size of the worker population, and therefore, persistence of the colony.

Behavioural effects of juvenile hormone and their influence on division of labour in leaf-cutting ant societies.

Division of labour in social insects represents a major evolutionary transition, but the physiological mechanisms that regulate this are still little understood. Experimental work with honey bees, and correlational analyses in other social insects, have implicated juvenile hormone (JH) as a regulatory factor, but direct experimental evidence of behavioural effects of JH in social insects is generally lacking. Here, we used experimental manipulation of JH to show that raised JH levels in leaf-cutting ants results in workers becoming more active, phototactic and threat responsive, and engaging in more extranidal activity - behavioural changes that we show are all characteristic of the transition from intranidal work to foraging. These behavioural effects on division of labour suggest that the JH mediation of behaviour occurs across multiple independent evolutions of eusociality, and may be a key endocrine regulator of the division of labour which has produced the remarkable ecological and evolutionary success of social insects.