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Background: The harmonious operation of many insect societies depends upon colony-wide dissemination of a non-volatile pheromone produced by a single queen, which informs workers of her presence. This represents a major challenge in large colonies. Honeybee colonies, which can exceed 60,000 bees, are believed to solve this challenge using 'messenger' workers that actively relay the queen pheromone throughout the hive. However, little is known about the structure and effectiveness of the underlying relay network or the biology of messaging., Results: Here, we combine automated tracking with modelling to address these outstanding questions. We find that both queen movement and worker messaging play fundamental roles in queen pheromone dissemination. Fine-grained analyses of worker behaviour confirmed the existence of active messaging, as physical contacts with the queen caused workers to move faster and straighter, thereby accelerating pheromone transmission. Finally, we show that messaging follows a stereotypical developmental trajectory, resulting in an age-dependent hierarchical relay network, with the most intense messaging observed between three and five days of age, when workers undergo a suite of physiological changes associated with queen rearing., Conclusions: These results suggest that the individuals that contribute most to advertising the presence of the queen are also the ones that control queen production., Competing Interests: Declarations. Ethics approval and consent to participate: Not applicable. Consent for publication: Not applicable. Competing interests: The authors declare that they have no competing interests., (© 2024. The Author(s).)

Contagious diseases are a major threat to societies in which individuals live in close contact. Social insects have evolved collective defense behaviors, such as social care or isolation of infected workers, that prevent outbreaks of pathogens. It has thus been suggested that individual immunity is reduced in species with such 'social immunity'. However, this hypothesis has not been tested functionally. Here, we characterize the immune response of the ant Lasius niger using a combination of genomic analysis, experimental infections, gene expression quantification, behavioural observations and pathogen quantifications. We uncover a striking specialization of immune responses towards different pathogens. Systemic individual immunity is effective against opportunistic bacterial infections, which are not covered by social immunity, but is not elicited upon fungal infections, which are effectively controlled by social immunity. This specialization suggests that immune layers have evolved complementary functions predicted to ensure the most cost-effective response against a wide range of pathogens., (© 2024. The Author(s).)

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.

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., (© 2022. The Author(s).)

Economic theory predicts that organisations achieve higher levels of productivity when tasks are divided among different subsets of workers. This prediction is based upon the expectation that individuals should perform best when they specialise upon a few tasks. However, in colonies of social insects evidence for a causal link between division of labour and performance is equivocal. To address this issue, we performed a targeted worker removal experiment to disrupt the normal allocation of workers to a cooperative team task - tandem running. During a tandem run a knowledgeable leader communicates the location of a new nest to a follower by physically guiding her there. The targeted removal of prominent leaders significantly reduced tandem performance, whereas removal of prominent followers had no effect. Furthermore, analyses of the experience of both participants in each tandem run revealed that tandem performance was influenced primarily by how consistently the leader acted as a leader when the need arose, but not by the consistency of the follower. Our study shows that performance in ant teams depends largely on whether or not a key role is filled by an experienced individual, and suggests that in animal teams, not all roles are equally important.

Spread of contagious pathogens critically depends on the number and types of contacts between infectious and susceptible hosts. Changes in social behavior by susceptible, exposed, or sick individuals thus have far-reaching downstream consequences for infectious disease spread. Although "social distancing" is now an all too familiar strategy for managing COVID-19, nonhuman animals also exhibit pathogen-induced changes in social interactions. Here, we synthesize the effects of infectious pathogens on social interactions in animals (including humans), review what is known about underlying mechanisms, and consider implications for evolution and epidemiology., (Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

Animal social networks are shaped by multiple selection pressures, including the need to ensure efficient communication and functioning while simultaneously limiting disease transmission. Social animals could potentially further reduce epidemic risk by altering their social networks in the presence of pathogens, yet there is currently no evidence for such pathogen-triggered responses. We tested this hypothesis experimentally in the ant Lasius niger using a combination of automated tracking, controlled pathogen exposure, transmission quantification, and temporally explicit simulations. Pathogen exposure induced behavioral changes in both exposed ants and their nestmates, which helped contain the disease by reinforcing key transmission-inhibitory properties of the colony's contact network. This suggests that social network plasticity in response to pathogens is an effective strategy for mitigating the effects of disease in social groups., (Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

Rhythmical activity patterns are ubiquitous in nature. We study an oscillatory biological system: collective activity cycles in ant colonies. Ant colonies have become model systems for research on biological networks because the interactions between the component parts are visible to the naked eye, and because the time-ordered contact network formed by these interactions serves as the substrate for the distribution of information and other resources throughout the colony. To understand how the collective activity cycles influence the contact network transport properties, we used an automated tracking system to record the movement of all the individuals within nine different ant colonies. From these trajectories we extracted over two million ant-to-ant interactions. Time-series analysis of the temporal fluctuations of the overall colony interaction and movement rates revealed that both the period and amplitude of the activity cycles exhibit a diurnal cycle, in which daytime cycles are faster and of greater amplitude than night cycles. Using epidemiology-derived models of transmission over networks, we compared the transmission properties of the observed periodic contact networks with those of synthetic aperiodic networks. These simulations revealed that contrary to some predictions, regularly-oscillating contact networks should impede information transmission. Further, we provide a mechanistic explanation for this effect, and present evidence in support of it.

Selection for disease control is believed to have contributed to shape the organisation of insect societies-leading to interaction patterns that mitigate disease transmission risk within colonies, conferring them 'organisational immunity'. Recent studies combining epidemiological models with social network analysis have identified general properties of interaction networks that may hinder propagation of infection within groups. These can be prophylactic and/or induced upon pathogen exposure. Here we review empirical evidence for these two types of organisational immunity in social insects and describe the individual-level behaviours that underlie it. We highlight areas requiring further investigation, and emphasise the need for tighter links between theory and empirical research and between individual-level and collective-level analyses., (Copyright © 2014 Elsevier Inc. All rights reserved.)

Self-organisation underlies many collective processes in large animal groups, where coordinated patterns and activities emerge at the group level from local interactions among its members. Although the importance of key individuals acting as effective leaders has recently been recognised in certain collective processes, it is widely believed that self-organised decisions are evenly shared among all or a subset of individuals acting as decision-makers, unless there are significant conflicts of interests among group members. Here, we show that certain individuals are disproportionately influential in self-organised decisions in a system where all individuals share the same interests: nest site selection by the ant Temnothorax albipennis. Workers that visited a good available nest site prior to emigration (the familiar nest) memorised its location, and later used this memory to navigate efficiently and find that nest faster than through random exploration. Additionally, these workers relied on their private information to expedite individual decisions about the familiar nest. This conferred a bias in favour of familiar nests over novel nests during emigrations. Informed workers were shown to have a significantly greater share in both recruitment and transport to the familiar nest than naïve workers. This suggests that they were the main determinants of the collective preference for familiar nests, and thus contributed greatly to enhance collective performance. Overall, these results indicate that self-organised decisions are not always evenly shared among decision-makers, even in systems where there are no conflicts of interest. Animal groups may instead benefit from well-informed, knowledgeable individuals acting as leaders in decisions.

Background: Successful collective decision-making depends on groups of animals being able to make accurate choices while maintaining group cohesion. However, increasing accuracy and/or cohesion usually decreases decision speed and vice-versa. Such trade-offs are widespread in animal decision-making and result in various decision-making strategies that emphasize either speed or accuracy, depending on the context. Speed-accuracy trade-offs have been the object of many theoretical investigations, but these studies did not consider the possible effects of previous experience and/or knowledge of individuals on such trade-offs. In this study, we investigated how previous knowledge of their environment may affect emigration speed, nest choice and colony cohesion in emigrations of the house-hunting ant Temnothorax albipennis, a collective decision-making process subject to a classical speed-accuracy trade-off., Methodology/principal Findings: Colonies allowed to explore a high quality nest site for one week before they were forced to emigrate found that nest and accepted it faster than emigrating naïve colonies. This resulted in increased speed in single choice emigrations and higher colony cohesion in binary choice emigrations. Additionally, colonies allowed to explore both high and low quality nest sites for one week prior to emigration remained more cohesive, made more accurate decisions and emigrated faster than emigrating naïve colonies., Conclusions/significance: These results show that colonies gather and store information about available nest sites while their nest is still intact, and later retrieve and use this information when they need to emigrate. This improves colony performance. Early gathering of information for later use is therefore an effective strategy allowing T. albipennis colonies to improve simultaneously all aspects of the decision-making process--i.e. speed, accuracy and cohesion--and partly circumvent the speed-accuracy trade-off classically observed during emigrations. These findings should be taken into account in future studies on speed-accuracy trade-offs.

Background: Timely decision making is crucial for survival and reproduction. Organisms often face a speed-accuracy trade-off, as fully informed, accurate decisions require time-consuming gathering and treatment of information. Optimal strategies for decision-making should therefore vary depending on the context. In mammals, there is mounting evidence that multiple systems of perceptual discrimination based on different neural circuits emphasize either fast responses or accurate treatment of stimuli depending on the context., Methodology/principal Findings: We used the ant Camponotus aethiops to test the prediction that fast information processing achieved through direct neural pathways should be favored in situations where quick reactions are adaptive. Social insects discriminate readily between harmless group-members and dangerous strangers using easily accessible cuticular hydrocarbons as nestmate recognition cues. We show that i) tethered ants display rapid aggressive reactions upon presentation of non-nestmate odor (120 to 160 ms); ii) ants' aggressiveness towards non-nestmates can be specifically reduced by exposure to non-nestmate odor only, showing that social interactions are not required to alter responses towards non-nestmates; iii) decision-making by ants does not require information transfer between brain hemispheres, but relies on side-specific decision rules., Conclusions/significance: Our results strongly suggest that first-order olfactory processing centers (up to the antennal lobes) are likely to play a key role in ant nestmate recognition. We hypothesize that the coarse level of discrimination achieved in the antennal lobes early in odor processing provides enough information to determine appropriate behavioral responses towards non-nestmates. This asks for a reappraisal of the mechanisms underlying social recognition in insects.