Social Insect Colonies Research Articles

Family before work: task reversion in workers of the red imported fire ant, Solenopsis invicta in the presence of brood

Among social insects, task allocation within its group members remains as one of the paramount pillars of social functionality. Division of labor in many eusocial insects is maintained by behavioral flexibility that can shift according to the needs of the colony they reside in. Workers typically, over time as they age, shift from intranidal nurses to extranidal foragers. If the needs of the colony change, either from the needs of the adults or the brood therein, workers shift their behavior in order to compensate for the need of a particular task to be done. This shift, either accelerating towards a behavior associated with an older worker, or regressing back into the nest, is not clearly understood in social insects outside of honeybees. In this study, evaluated how brood type affected the red imported fire ant, Solenopsis invicta, worker task reversion and acceleration. Through observation of worker behaviors performed over multiple time-points per day, we discovered that worker task reversion and acceleration does occur within this ant species. Furthermore, the type of brood influenced the rate at which this occurred, with larvae having the strongest effect of all types. Finally, there was a propensity for workers to maintain their new behavior throughout the experiment. This study shows that the needs of brood within a social insect colony can influence the behavior workers perform, reversing the age polyethism that is common among social insect species.

Scaling of ant colony interaction networks

In social insect colonies, individuals are physically independent but functionally integrated by interaction networks which provide a foundation for communication and drive the emergence of collective behaviors, including nest architecture, division of labor, and potentially also the social regulation of metabolic rates. To investigate the relationship between interactions, metabolism, and colony size, we varied group size for harvester ant colonies (Pogonomyrmex californicus) and assessed their communication networks based on direct antennal contacts and compared these results with proximity networks and a random movement simulation. We found support for the hypothesis of social regulation; individuals did not interact with each other randomly but exhibited restraint. Connectivity scaled hypometrically with colony size, per-capita interaction rate was scale-invariant, and smaller colonies exhibited higher measures of closeness centrality and edge density, correlating with higher per-capita metabolic rates. Although the immediate energetic cost for two ants to interact is insignificant, the downstream effects of receiving and integrating social information can have metabolic consequences. Our results indicate that individuals in larger colonies are relatively more insulated from each other, a factor that may reduce or filter noisy stimuli and contribute to the hypometric scaling of their metabolic rates, and perhaps more generally, the evolution of larger colony sizes.

Surplus feeding reverses worker ovarian suppression and disrupts social cohesion in queen-right wasp colonies

Nutrition is an important component of oogenesis and ovarian development in insects. In social insect colonies where a large proportion of females are sterile, suppression of reproduction caused by differential acquisition and retention of nutrition has been hypothesized to cause worker sterility. This study, using the primitively eusocial wasp Ropalidia marginata (Lepeletier) (Hymenoptera: Vespidae), show that worker ovarian development in naturally foraging colonies is more similar to experimentally food-limited colonies than to surplus-fed colonies, indicating nutritional castration in workers whose ovaries are inhibited by food availability. Further, experimental provisioning of surplus nutrition led to higher ovarian development in workers as compared to naturally foraging and food-limited workers. Surplus feeding also led to higher nest desertion by workers, leading to a breakdown of the colony’s social structure, whereas food-limited colonies retained workers.

A mathematical framework for collective foraging behavior of social insect colonies in multi-dynamic environments

Understanding collective behavior is integral to disciplines including developmental biology, behavioral ecology, and sociology. In this investigation, we construct deterministic and stochastic models for exploring how internal factors (i.e., task demand) and external factors (i.e., dynamic environment) drive the collective foraging behavior of social insect colonies. Through theoretical analysis, we demonstrate the global stability of an interior equilibrium for the deterministic case, and study the existence of a unique stationary distribution for the stochastic case. Surprisingly, the global stability of the interior equilibrium and the existence of a unique stationary distribution of the proposed models do not depend on additional conditions. The main contribution of this work is to construct a new mathematical framework to explore the influence of internal stimulus and external fluctuation on the dynamics of social insect colonies, and to provide corresponding theoretical analysis methods.

Field-realistic concentrations of a neonicotinoid insecticide influence socially regulated brood development in a bumblebee.

The systemic neonicotinoid insecticides are considered as one of the key culprits contributing to ongoing declines in pollinator health and abundance. Bumblebees are among the most important pollinators of temperate zone plants, making their susceptibility to neonicotinoid exposure of great concern. We report that bumblebee (Bombus terrestris) colonies exposed to field-realistic concentrations of the commonly used neonicotinoid Imidacloprid grew slower, consumed less food, and produced fewer workers, males and gynes, but unexpectedly produced larger workers compared to control colonies. Behavioural observations show that queens in pesticide-treated colonies spend more time inactive and less time caring for the brood. We suggest that the observed effects on brood body size are driven by a decreased queen ability to manipulate the larva developmental programme. These findings reveal an intricate and previously unknown effect of insecticides on the social interactions controlling brood development in social insect colonies. Insecticide influences on the social mechanisms regulating larval development are potentially detrimental for bumblebees, in which body size strongly influences both caste differentiation and the division of labour among workers, two organization principles of insect societies.

A Collective Colony Migration Model with Hill Functions in Recruitment

Social insect colonies’ robust and efficient collective behaviors without any central control contribute greatly to their ecological success. Colony migration is a leading subject for studying collective decision-making in migration. In this paper, a general colony migration model with Hill functions in recruitment is proposed to investigate the underlying decision making mechanism and the related dynamical behaviors. Our analysis provides the existence and stability of equilibrium, and the global dynamical behavior of the system. To understand how piecewise functions and Hill functions in recruitment impact colony migration dynamics, the comparisons are performed in both analytic results and bifurcation analysis. Our theoretical results show that the dynamics of the migration system with Hill functions in recruitment differs from that of the migration system with piecewise functions in the following three aspects: (1) all population components in our colony migration model with Hill functions in recruitment are persistent; (2) the colony migration model with Hill functions in recruitment has saddle and saddle-node bifurcations, while the migration system with piecewise functions does not; (3) the system with Hill functions has only equilibrium dynamics, i.e. either has a global stability at one interior equilibrium or has bistablity among two locally stable interior equilibria. Bifurcation analysis shows that the geometrical shape of the Hill functions greatly impacts the dynamics: (1) the system with flatter Hill functions is less likely to exhibit bistability; (2) the system with steeper functions is prone to exhibit bistability, and the steady state of total active workers is closer to that of active workers in the system with piecewise function.

Metabolic rate shapes differences in foraging efficiency among honeybee foragers

Abstract Metabolic rate is the rate at which organisms process energy and is often considered as the fundamental driver of life history processes. The link between metabolic rate and life history is critically mediated via foraging, which shapes the energy acquisition patterns of an individual. This predicts that individuals with different metabolic rates likely vary in their foraging strategies, although such a link has rarely been empirically investigated in the context of optimal foraging theory—a powerful framework for understanding how animals maximize their foraging returns. Many central place foragers such as honeybees maximize their energetic efficiency rather than the rate of energetic gain, given the critical role of energetic costs in foraging decisions. We therefore tested if individuals with low and high metabolic rates differ in efficiency maximization, using genetic lines of honeybees with different metabolic rates. Our results show that low metabolic rate foragers visit more flowers during a foraging trip and have a higher energetic efficiency than high metabolic rate foragers in both low and high resource conditions. We discuss the significance of these results in the context of division of labor and the adaptive role of phenotypic diversity in metabolic rate in a social insect colony.

Transcriptomics on Social Interactions in Termites: Effects of Soldier Presence

The organization of social insect colonies requires sophisticated mechanisms to regulate caste composition according to colony demands. In termites, the soldier caste is responsible for the inhibition of soldier differentiation, but the mechanism underlying the regulation of soldier differentiation is still unclear. In this study, we performed transcriptome analyses to identify genes expressed in workers that fluctuated in the presence of soldiers in the subterranean termite Reticulitermes speratus. First, soldier differentiation was artificially induced via juvenile hormone (JH) application, and the inhibitory effects of soldier differentiation on soldier presence were evaluated. Second, transcriptomes were prepared from workers with or without soldiers under JH treatment, and expression analyses were performed to identify differentially expressed genes (DEGs) for each treatment. The expression levels of several DEGs were verified by quantitative real-time PCR. The results indicated that only a small number of DEGs were upregulated by the presence of soldiers. A homology search of DEGs and gene ontology (GO) analysis of the DEGs showed that some genes were responsible for the regulation of hormone levels, social interaction, and response to xenobiotic substances, suggesting that they could be involved in developmental arrest and pheromonal regulation in workers. Moreover, GO analysis indicated that the expression of many genes, including those involved in hormone metabolic processes, fluctuated with JH application. Suppression of soldier differentiation in the presence of soldiers could be accomplished by the expression of a large number of genes required for soldier differentiation.

Rescue Strategy in a Termite: Workers Exposed to a Fungal Pathogen Are Reintegrated Into the Colony

Social insect colonies are characterized by an efficient division of labor, allowing high-value individuals (i.e., reproductives and brood) to be sheltered from tasks associated with increased risk of pathogen exposure, such as foraging or corpse disposal. This social organization helps limit the transmission of disease throughout the colony. Further, individuals can actively respond to imminent disease threats by altering their behaviors as a means of social immunity. In subterranean termites, although workers typically avoid detected pathogens, they can be attracted to pathogen cues when a nestmate is infected. Infected termites are usually groomed, but they may instead be cannibalized if the infection has already become lethal. The mechanisms governing these changes in behavior are unclear. We set out to examine immediate changes in individual behaviors, investigating the role that the infected individual plays in communicating its infection status to nestmates. We also assessed gradual changes in social organization after the re-introduction of an infected termite to the colony. Our results reveal that infected termites likely do not signal their infection status to nestmates through shaking behaviors and reduced movements, suggesting the occurrence of other mechanisms used in communicating infection. We also found that infected termites do not self-isolate and may travel to the densest part of the colony, where they can potentially benefit from grooming by large groups of nestmates. These results provide new insights into how individual changes in immune behaviors contribute to overall colony health, highlighting that, at early stages of infection, termites favor a rescuing strategy rather than isolation and/or cannibalization.

Negative feedback may suppress variation to improve collective foraging performance.

Social insect colonies use negative as well as positive feedback signals to regulate foraging behaviour. In ants and bees individual foragers have been observed to use negative pheromones or mechano-auditory signals to indicate that forage sources are not ideal, for example being unrewarded, crowded, or dangerous. Here we propose an additional function for negative feedback signals during foraging, variance reduction. We show that while on average populations will converge to desired distributions over forage patches both with and without negative feedback signals, in small populations negative feedback reduces variation around the target distribution compared to the use of positive feedback alone. Our results are independent of the nature of the target distribution, providing it can be achieved by foragers collecting only local information. Since robustness is a key aim for biological systems, and deviation from target foraging distributions may be costly, we argue that this could be a further important and hitherto overlooked reason that negative feedback signals are used by foraging social insects.

Colony-Level Viral Load Influences Collective Foraging in Honey Bees.

Nutrition is an important component of social insect colony health especially in the face of stressors such as parasitism and viral infections. Honey bees are known to preferentially select nectar and pollen based on macronutrient and phytochemical contents and in response to pathogen loads. However, given that honey bees live in colonies, collective foraging decisions may be impacted directly by forager infection status but also by colony health. This field experiment was conducted to determine if honey bee viral infections are correlated with pollen and nectar foraging and if these associations are impacted more by colony or forager infection. By comparing regressions with and without forager and colony variables and through structural equation models, we were able to determine the relative contributions of colony and forager virus loads on forager decisions. We found that foragers had higher numbers and levels of BQCV and CBPV but lower levels of DWV viruses than their respective colonies. Overall, individuals appeared to forage based a combination of their own and colony health but with greater weight given to colony metrics. Colony parasitism by Varroa mites, positively correlated with both forager and colony DWV-B levels, was negatively associated with nectar weight. Further, colony DWV-B levels were negatively associated with individually foraged pollen protein: lipid ratios but positively correlated with nectar weight and sugar content. This study shows that both colony and forager health can simultaneously mediate individual foraging decisions and that the importance of viral infections and parasite levels varies with foraging metrics. Overall, this work highlights the continued need to explore the interactions of disease, nutrition, and genetics in social interactions and structures.

Conflicting selection on workers underlies global honey bee colony losses

There is clear evidence for global and unsustainable high losses of the managed Western honey bee, Apis mellifera, colonies raising major concerns about the sustainability of pollination services and food security. Here, we address a conflicting selection scenario in workers to better understand life-history trade-offs underlying colony losses. Due to developmental plasticity, annual fluctuations in selection pressures result in long-living winter bees and short-living summer bees as adaptive responses to lack of food and ceased brood rearing in winter, or ample food and rapid brood turnover in spring and summer. Since trait evolution is governed by a balance of conflicting fitness advantages, trade-offs between longevity and other traits are inevitable (e.g. immune defense or detoxification). As worker longevity is essential to ensure colony functionality, these trade-offs render long-living workers more susceptible to the same stressors compared to short-lived ones. It seems as if trade-offs in workers play a previously overlooked key role, and the incorporation of long-living workers in research efforts is long overdue if our aim is to effectively mitigate declines and losses of social insect colonies globally. Indeed, managed honey bee colony losses in temperate regions predominantly occur throughout winter, but research efforts are almost exclusively conducted with short-lived summer bees, thereby sustaining the danger of false negative results. Thus, we should not shy away from meeting the respective logistic challenges. Studies of conflicting selection on workers will be informative about mechanisms underlying life history trade-offs, thereby fostering conservation efforts in the social insects.

When being flexible matters: Ecological underpinnings for the evolution of collective flexibility and task allocation

Task allocation is a central feature of collective organization. Living collective systems, such as multicellular organisms or social insect colonies, have evolved diverse ways to allocate individuals to different tasks, ranging from rigid, inflexible task allocation that is not adjusted to changing circumstances to more fluid, flexible task allocation that is rapidly adjusted to the external environment. While the mechanisms underlying task allocation have been intensely studied, it remains poorly understood whether differences in the flexibility of task allocation can be viewed as adaptive responses to different ecological contexts—for example, different degrees of temporal variability. Motivated by this question, we develop an analytically tractable mathematical framework to explore the evolution of task allocation in dynamic environments. We find that collective flexibility is not necessarily always adaptive, and fails to evolve in environments that change too slowly (relative to how long tasks can be left unattended) or too quickly (relative to how rapidly task allocation can be adjusted). We further employ the framework to investigate how environmental variability impacts the internal organization of task allocation, which allows us to propose adaptive explanations for some puzzling empirical observations, such as seemingly unnecessary task switching under constant environmental conditions, apparent task specialization without efficiency benefits, and high levels of individual inactivity. Altogether, this work provides a general framework for probing the evolved diversity of task allocation strategies in nature and reinforces the idea that considering a system’s ecology is crucial to explaining its collective organization.

Social insect colony size is correlated with rates of molecular evolution

Social insect colony size is correlated with rates of molecular evolution

Division of foraging behaviour: Assessments of pollinator traits when visiting a model plant species

Diverse animals visit flowers but not all engage in pollination, and only behaviours involving stigmal contact result in successful pollination events. Ethological indices developed for sociobiological contexts (caste evolution) have unrealized potential to provide insights on pollination services but have not been applied in this context before. In the present study, we characterized foraging behaviours as functional traits, which allowed us to predict whether ecosystems services are robust to species-specific trait loss. We aimed to (1) document the variety, duration and frequency of on-flower behaviours, (2) determine which taxa engage in stigmal contact and (3) investigate vulnerabilities of pollination service to loss of pollinator taxa. We used video recordings to document on-flower behaviours of animals visiting a single apple cultivar (Malus domestica var. ‘Pink Lady’), which removed confounding factors to enable a robust assessment of functional pollination behaviour. We adapted division of labour statistics (designed to assess caste-specific behavioural task fidelity within social insect colonies) to investigate taxon-specific foraging behaviours within this assemblage of pollinators – a novel application. An ethogram of 11 behaviours was derived from 19,518 min of observations (2350 visits; 19 taxa). Most (53%) flower visits involved stigmal contact (termed ‘contact visits’), but the percentage of contact visits varied between taxa. We introduce division of foraging behaviour (DFB) indices – which imply the focal pollinator assemblage consists of a mix of behaviourally generalized and specialized taxa with a slight bias towards specialization: division of taxa into behaviours DFBY|X = 0.59; division of behaviours into taxa DFBX|Y = 0.76. Simulated extinction of taxa from this insect assemblage significantly shifted DFBY|X in four instances. These qualitative assessments of behavioural traits imply moderate functional redundancy in pollination services provided by 11 insect taxa to a model plant, even under simulated extinction events, suggesting pollination services may be somewhat resilient to animal–plant network disruptions in this Australian agroecological study system.

Hierarchy Establishment from Nonlinear Social Interactions and Metabolic Costs: An Application to Harpegnathos saltator

Social hierarchies are ubiquitous in social groups such as human societies and social insect colonies; however, the factors that maintain these hierarchies are less clear. Motivated by the shared reproductive hierarchy of the ant species Harpegnathos saltator, we have developed simple compartmental nonlinear differential equations to explore how key life-history and metabolic rate parameters may impact and determine its colony size and the length of its shared hierarchy. Our modeling approach incorporates nonlinear social interactions and metabolic theory. The results from the proposed model, which were linked with limited data, show that: (1) the proportion of reproductive individuals decreases over colony growth; (2) an increase in mortality rates can diminish colony size but may also increase the proportion of reproductive individuals; and (3) the metabolic rates have a major impact in the colony size and structure of a shared hierarchy.

Unbalanced fatty acid diets impair discrimination ability of honey bee workers to damaged and healthy brood odors.

Nutrition supports social insect colonies by regulating both individual performance and colony growth. In honey bee colonies, task-related behaviors such as nursing and foraging are partially mediated by nutrition. Young workers (nurses) consume almost all of the pollen in the hive, while foragers consume mostly nectar. Pollen provides vital proteins and lipids, consumed by nurse bees for approximately 1week post-eclosion. The role that lipids play in the physiology and behavior of adult bees is gaining significant attention. Recent research suggests that diets with balanced ratios of fatty acids increase olfactory learning in honey bees. Olfaction is crucial for young worker bees to perform brood care and cell cleaning behaviors, which is important for hive health and disease control. Thus, we targeted the early adult, pollen-feeding stage to examine how fatty acids affect cognition to hive-relevant odors. We fed young workers (days 0-9) diets balanced or unbalanced in their ratio of essential fatty acids (ω-6:3) sourced from pollen or cooking oils. We then measured their ability to learn healthy and damaged brood odors, as well as their ability to discriminate between the two. Workers fed balanced diets could learn and discriminate between brood odors better than workers fed unbalanced diets. Consumption of both diet types decreased with age, but their cognitive effects remained. These results suggest that diet affects young worker cognitive development, which may affect task-related behaviors and colony hygiene.

Termite nest evolution fostered social parasitism by termitophilous rove beetles.

Colonies of social insects contain large amounts of resources often exploited by specialized social parasites. Although some termite species host numerous parasitic arthropod species, called termitophiles, others host none. The reason for this large variability remains unknown. Here, we report that the evolution of termitophily in rove beetles is linked to termite nesting strategies. We compared one‐piece nesters, whose entire colony life is completed within a single wood piece, to foraging species, which exploit multiple physically separated food sources. Our epidemiological model predicts that characteristics related to foraging (e.g., extended colony longevity and frequent interactions with other colonies) increase the probability of parasitism by termitophiles. We tested our prediction using literature data. We found that foraging species are more likely to host termitophilous rove beetles than one‐piece nesters: 99.6% of known termitophilous species were associated with foraging termites, whereas 0.4% were associated with one‐piece nesters. Notably, the few one‐piece nesting species hosting termitophiles were those having foraging potential and access to soil. Our phylogenetic analyses confirmed that termitophily primarily evolved with foraging termites. These results highlight that the evolution of complex termite societies fostered social parasitism, explaining why some species have more social parasites than others.

Effects of environmental stochasticity on the foraging dynamics of ant colonies driven by physical interactions

Collective foraging is critical for the ecological and evolutionary success of social insect colonies. To evaluate the impact of environmental stochasticity on the collective foraging dynamics of social ants, this paper develops a collective foraging model based on stochastic differential equations, in which communication among workers mainly relies on physical interactions. By analyzing the stochastic dynamics of the constructed model, we obtain relaxation conditions for the existence of an ergodic stationary distribution. Theoretical results suggest that environmental stochasticity leads to a decrease in the effective recruitment rate and average foraging period of foragers, ultimately negatively affecting the average recruit recruitment ability of single returning forager.

A Gland of Many Uses: a Diversity of Compounds in the Labial Glands of the Bumble Bee Bombus impatiens Suggests Multiple Signaling Functions.

Communication in social insect colonies depends on signals accurately reflecting the identity and physiological state of the individuals. Such information is coded by the products of multiple exocrine glands, and the resulting blends reflect the species, sex, caste, age, task, reproductive status, and health of an individual, and may also contain caste-specific pheromones regulating the behavior and physiology of other individuals. Here we examined the composition of labial gland secretions in females of the bumble bee Bombus impatiens, of different castes, social condition, age, mating status, and ovarian activation. We show that active queens, gynes, and workers each produce caste-specific compounds that may serve different communicative functions. The composition and amounts of wax esters, mostly octyl esters produced by active queens, differed significantly between castes, mating, and social conditions, suggesting a social signaling role. Farnesyl esters were predominant in gynes and peaked at optimal mating age (6-10days), suggesting their possible roles as sex pheromone components. Reproductive status of females and age across castes was reflected by the ratio between short- and long-chain hydrocarbons, suggesting that these compounds may serve as fertility signals. Our findings overall suggest that the labial gland composition in B. impatiens reflects different facets of female physiology. While further bioassays are required to determine the functions of these compounds, they are likely to have important roles in communication between individuals.