Social network position is a major predictor of ant behavior, microbiota composition, and brain gene expression.

The physiology and behavior of social organisms correlate with their social environments. However, because social environments are typically confounded by age and physical environments (i.e., spatial location and associated abiotic factors), these correlations are usually difficult to interpret. For example, associations between an individual's social environment and its gene expression patterns may result from both factors being driven by age or behavior. Simultaneous measurement of pertinent variables and quantification of the correlations between these variables can indicate whether relationships are direct (and possibly causal) or indirect. Here, we combine demographic and automated behavioral tracking with a multiomic approach to dissect the correlation structure among the social and physical environment, age, behavior, brain gene expression, and microbiota composition in the carpenter ant Camponotus fellah. Variations in physiology and behavior were most strongly correlated with the social environment. Moreover, seemingly strong correlations between brain gene expression and microbiota composition, physical environment, age, and behavior became weak when controlling for the social environment. Consistent with this, a machine learning analysis revealed that from brain gene expression data, an individual's social environment can be more accurately predicted than any other behavioral metric. These results indicate that social environment is a key regulator of behavior and physiology.

Functional and mechanistic diversity in ant tandem communication.

Communication is fundamental to the organization of animal societies, often resulting in the convergent evolution of similar social behavior across lineages. However, this similarity may conceal underlying functional and mechanistic differences. Here we combined network and information-theoretic analysis to quantify how tandem recruitment is distinguishable between two ant genera, Temnothorax and Diacamma. We show that Temnothorax uses tandem running to recruit additional recruiters, while Diacamma uses it principally to move the passive majority of their colony, a task that Temnothorax accomplishes with a different behavior, social carrying. Accordingly, the network structure of Diacamma tandems was dissimilar to that of Temnothorax, instead resembling the social-carrying networks in Temnothorax. Furthermore, our information-theoretical analysis on movement trajectories revealed that Diacamma tandem runs lack bidirectional information transfer, the signature of route learning in Temnothorax. By quantifying the diversity of similar communication systems, this study increases the resolution of our understanding of animal societies.

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.

The gut microbiota affects the social network of honeybees.

The gut microbiota influences animal neurodevelopment and behaviour but has not previously been documented to affect group-level properties of social organisms. Here, we use honeybees to probe the effect of the gut microbiota on host social behaviour. We found that the microbiota increased the rate and specialization of head-to-head interactions between bees. Microbiota colonization was associated with higher abundances of one-third of the metabolites detected in the brain, including amino acids with roles in synaptic transmission and brain energetic function. Some of these metabolites were significant predictors of the number of social interactions. Microbiota colonization also affected brain transcriptional processes related to amino acid metabolism and epigenetic modifications in a brain region involved in sensory perception. These results demonstrate that the gut microbiota modulates the emergent colony social network of honeybees and suggest changes in chromatin accessibility and amino acid biosynthesis as underlying processes.

Leadership - not followership - determines performance in ant teams.

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.

Ant behavioral maturation is mediated by a stochastic transition between two fundamental states.

The remarkable ecological success of social insects is often attributed to their advanced division of labor, which is closely associated with temporal polyethism in which workers transition between different tasks as they age. Young nurses are typically found deep within the nest where they tend to the queen and the brood, whereas older foragers are found near the entrance and outside the nest.1-3 However, the individual-level maturation dynamics remain poorly understood because following individuals over relevant timescales is difficult; hence, previous experimental studies used same-age cohort designs.4-15 To address this, we used an automated tracking system to follow >500 individuals over >100 days and constructed networks of physical contacts to provide a continuous measure of worker social maturity. These analyses revealed that most workers occupied one of two steady states, namely a low-maturity nurse state and a high-maturity forager state, with the remaining workers rapidly transitioning between these states. There was considerable variation in the age at transition, and, surprisingly, the transition probability was age independent. This suggests that the transition is largely stochastic rather than a hard-wired age-dependent physiological change. Despite the variation in timing, the transition dynamics were highly stereotyped. Transitioning workers moved from the nurse to the forager state according to an S-shaped trajectory, and only began foraging after completing the transition. Stochastic switching, which occurs in many other biological systems, may provide ant colonies with robustness to extrinsic perturbations by allowing the colony to decouple its division of labor from its demography.

The influence of the few: a stable 'oligarchy' controls information flow in house-hunting ants.

Animals that live together in groups often face difficult choices, such as which food resource to exploit, or which direction to flee in response to a predator. When there are costs associated with deadlock or group fragmentation, it is essential that the group achieves a consensus decision. Here, we study consensus formation in emigrating ant colonies faced with a binary choice between two identical nest-sites. By individually tagging each ant with a unique radio-frequency identification microchip, and then recording all ant-to-ant 'tandem runs'-stereotyped physical interactions that communicate information about potential nest-sites-we assembled the networks that trace the spread of consensus throughout the colony. Through repeated emigrations, we show that both the order in which these networks are assembled and the position of each individual within them are consistent from emigration to emigration. We demonstrate that the formation of the consensus is delegated to an influential but exclusive minority of highly active individuals-an 'oligarchy'-which is further divided into two subgroups, each specialized upon a different tandem running role. Finally, we show that communication primarily occurs between subgroups not within them, and further, that such between-group communication is more efficient than within-group communication.

Measuring site fidelity and spatial segregation within animal societies.

Animals often display a marked tendency to return to previously visited locations that contain important resources, such as water, food, or developing brood that must be provisioned. A considerable body of work has demonstrated that this tendency is strongly expressed in ants, which exhibit fidelity to particular sites both inside and outside the nest. However, thus far many studies of this phenomena have taken the approach of reducing an animal's trajectory to a summary statistic, such as the area it covers.Using both simulations of biased random walks, and empirical trajectories from individual rock ants, Temnothorax albipennis, we demonstrate that this reductive approach suffers from an unacceptably high rate of false negatives.To overcome this, we describe a site-centric approach which, in combination with a spatially-explicit null model, allows the identification of the important sites towards which individuals exhibit statistically significant biases.Using the ant trajectories, we illustrate how the site-centric approach can be combined with social network analysis tools to detect groups of individuals whose members display similar space-use patterns.We also address the mechanistic origin of individual site fidelity; by examining the sequence of visits to each site, we detect a statistical signature associated with a self-attracting walk - a non-Markovian movement model that has been suggested as a possible mechanism for generating individual site fidelity.

Short-term activity cycles impede information transmission in ant colonies.

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.

Beyond contact-based transmission networks: the role of spatial coincidence.

Animal societies rely on interactions between group members to effectively communicate and coordinate their actions. To date, the transmission properties of interaction networks formed by direct physical contacts have been extensively studied for many animal societies and in all cases found to inhibit spreading. Such direct interactions do not, however, represent the only viable pathways. When spreading agents can persist in the environment, indirect transmission via 'same-place, different-time' spatial coincidences becomes possible. Previous studies have neglected these indirect pathways and their role in transmission. Here, we use rock ant colonies, a model social species whose flat nest geometry, coupled with individually tagged workers, allowed us to build temporally and spatially explicit interaction networks in which edges represent either direct physical contacts or indirect spatial coincidences. We show how the addition of indirect pathways allows the network to enhance or inhibit the spreading of different types of agent. This dual-functionality arises from an interplay between the interaction-strength distribution generated by the ants' movement and environmental decay characteristics of the spreading agent. These findings offer a general mechanism for understanding how interaction patterns might be tuned in animal societies to control the simultaneous transmission of harmful and beneficial agents.

Ant search strategies after interrupted tandem runs.

Tandem runs are a form of recruitment in ants. During a tandem run, a single leader teaches one follower the route to important resources such as sources of food or better nest sites. In the present study, we investigate what tandem leaders and followers do, in the context of nest emigration, if their partner goes missing. Our experiments involved removing either leaders or followers at set points during tandem runs. Former leaders first stand still and wait for their missing follower but then most often proceed alone to the new nest site. By contrast, former followers often first engage in a Brownian search, for almost exactly the time that their former leader should have waited for them, and then former followers switch to a superdiffusive search. In this way, former followers first search their immediate neighbourhood for their lost leader before becoming ever more wide ranging so that in the absence of their former leader they can often find the new nest, re-encounter the old one or meet a new leader. We also show that followers gain useful information even from incomplete tandem runs. These observations point to the important principle that sophisticated communication behaviours may have evolved as anytime algorithms, i.e. procedures that are beneficial even if they do not run to completion.

Record dynamics in ants.

The success of social animals (including ourselves) can be attributed to efficiencies that arise from a division of labour. Many animal societies have a communal nest which certain individuals must leave to perform external tasks, for example foraging or patrolling. Staying at home to care for young or leaving to find food is one of the most fundamental divisions of labour. It is also often a choice between safety and danger. Here we explore the regulation of departures from ant nests. We consider the extreme situation in which no one returns and show experimentally that exiting decisions seem to be governed by fluctuating record signals and ant-ant interactions. A record signal is a new 'high water mark' in the history of a system. An ant exiting the nest only when the record signal reaches a level it has never perceived before could be a very effective mechanism to postpone, until the last possible moment, a potentially fatal decision. We also show that record dynamics may be involved in first exits by individually tagged ants even when their nest mates are allowed to re-enter the nest. So record dynamics may play a role in allocating individuals to tasks, both in emergencies and in everyday life. The dynamics of several complex but purely physical systems are also based on record signals but this is the first time they have been experimentally shown in a biological system.

Teaching with evaluation in ants.

Tandem running in ants is a form of recruitment in which a single well-informed worker guides a naive nestmate to a goal [1-8]. The ant Temnothorax albipennis recently satisfied a strict set of predefined criteria for teaching in nonhuman animals [9, 10]. These criteria do not include evaluation as a prerequisite for teaching [10]. However, some authors claim that true teaching is always evaluative, i.e., sensitive to the competence or quality of the pupil [11-13]. They then assume, on the premise that only humans are capable of making such necessarily complex cognitive evaluations, that teaching must be unique to humans. We conducted experiments to test whether evaluation occurs during tandem running, in which a knowledgeable ant physically guides a naive follower to a goal. In each experiment, we interrupted the tandem run by removing the tandem follower. The response of the leader was to stand still at the point where the tandem run was interrupted. We then measured how long the leader waited for the missing follower before giving up. Our results demonstrate T. albipennis performs three different kinds of evaluation. First, the longer the tandem has proceeded the longer the leader will wait for the follower to re-establish contact. Second, ant teachers modulate their giving-up time depending on the value of the goal. Finally, leaders have shorter giving-up times after unusually slow tandem runs.