Rationality in collective decision-making by ant colonies

Economic models of animal behaviour assume that decision-makers are rational, meaning that they assess options according to intrinsic fitness value and not by comparison with available alternatives. This expectation is frequently violated, but the significance of irrational behaviour remains controversial. One possibility is that irrationality arises from cognitive constraints that necessitate short cuts like comparative evaluation. If so, the study of whether and when irrationality occurs can illuminate cognitive mechanisms. We applied this logic in a novel setting: the collective decisions of insect societies. We tested for irrationality in colonies of Temnothorax ants choosing between two nest sites that varied in multiple attributes, such that neither site was clearly superior. In similar situations, individual animals show irrational changes in preference when a third relatively unattractive option is introduced. In contrast, we found no such effect in colonies. We suggest that immunity to irrationality in this case may result from the ants’ decentralized decision mechanism. A colony''s choice does not depend on site comparison by individuals, but instead self-organizes from the interactions of multiple ants, most of which are aware of only a single site. This strategy may filter out comparative effects, preventing systematic errors that would otherwise arise from the cognitive limitations of individuals.     

Social transfer of pathogenic fungus promotes active immunisation in ant colonies

Due to the omnipresent risk of epidemics, insect societies have evolved sophisticated disease defences at the individual and colony level. An intriguing yet little understood phenomenon is that social contact to pathogen-exposed individuals reduces susceptibility of previously naive nestmates to this pathogen. We tested whether such social immunisation in Lasius ants against the entomopathogenic fungus Metarhizium anisopliae is based on active upregulation of the immune system of nestmates following contact to an infectious individual or passive protection via transfer of immune effectors among group members--that is, active versus passive immunisation. We found no evidence for involvement of passive immunisation via transfer of antimicrobials among colony members. Instead, intensive allogrooming behaviour between naive and pathogen-exposed ants before fungal conidia firmly attached to their cuticle suggested passage of the pathogen from the exposed individuals to their nestmates. By tracing fluorescence-labelled conidia we indeed detected frequent pathogen transfer to the nestmates, where they caused low-level infections as revealed by growth of small numbers of fungal colony forming units from their dissected body content. These infections rarely led to death, but instead promoted an enhanced ability to inhibit fungal growth and an active upregulation of immune genes involved in antifungal defences (defensin and prophenoloxidase, PPO). Contrarily, there was no upregulation of the gene cathepsin L, which is associated with antibacterial and antiviral defences, and we found no increased antibacterial activity of nestmates of fungus-exposed ants. This indicates that social immunisation after fungal exposure is specific, similar to recent findings for individual-level immune priming in invertebrates. Epidemiological modeling further suggests that active social immunisation is adaptive, as it leads to faster elimination of the disease and lower death rates than passive immunisation. Interestingly, humans have also utilised the protective effect of low-level infections to fight smallpox by intentional transfer of low pathogen doses ("variolation" or "inoculation").     

Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus

In social insects, group behaviour can increase disease resistance among nest-mates and generate social prophylaxis. Stomodeal trophallaxis, or mutual feeding through regurgitation, may boost colony-level immunocompetence. We provide evidence for increased trophallactic behaviour among immunized workers of the carpenter ant Camponotus pennsylvanicus, which, together with increased antimicrobial activity of the regurgitate droplet, help explain the improved survival of droplet recipient ants relative to controls following an immune challenge. We have identified a protein related to cathepsin D, a lysosomal protease, as a potential contributor to the antimicrobial activity. The combined behavioural and immunological responses to infection in these ants probably represent an effective mechanism underlying the social facilitation of disease resistance, which could potentially produce socially mediated colony-wide prophylaxis. The externalization and sharing of an individual''s immune responses via trophallaxis could be an important component of social immunity, allowing insect colonies to thrive under high pathogenic pressures.     

Characterizing the collective personality of ant societies: aggressive colonies do not abandon their home

Animal groups can show consistent behaviors or personalities just like solitary animals. We studied the collective behavior of Temnothorax nylanderi ant colonies, including consistency in behavior and correlations between different behavioral traits. We focused on four collective behaviors (aggression against intruders, nest relocation, removal of infected corpses and nest reconstruction) and also tested for links to the immune defense level of a colony and a fitness component (per-capita productivity). Behaviors leading to an increased exposure of ants to micro-parasites were expected to be positively associated with immune defense measures and indeed colonies that often relocated to other nest sites showed increased immune defense levels. Besides, colonies that responded with low aggression to intruders or failed to remove infected corpses, showed a higher likelihood to move to a new nest site. This resembles the trade-off between aggression and relocation often observed in solitary animals. Finally, one of the behaviors, nest reconstruction, was positively linked to per-capita productivity, whereas other colony-level behaviors, such as aggression against intruders, showed no association, albeit all behaviors were expected to be important for fitness under field conditions. In summary, our study shows that ant societies exhibit complex personalities that can be associated to the physiology and fitness of the colony. Some of these behaviors are linked in suites of correlated behaviors, similar to personalities of solitary animals.     

Social influence on age and reproduction: reduced lifespan and fecundity in multi-queen ant colonies

Evolutionary theories of ageing predict that life span increases with decreasing extrinsic mortality, and life span variation among queens in ant species seems to corroborate this prediction: queens, which are the only reproductive in a colony, live much longer than queens in multi-queen colonies. The latter often inhabit ephemeral nest sites and accordingly are assumed to experience a higher mortality risk. Yet, all prior studies compared queens from different single- and multi-queen species. Here, we demonstrate an effect of queen number on longevity and fecundity within a single, socially plastic species, where queens experience the similar level of extrinsic mortality. Queens from single- and two-queen colonies had significantly longer lifespan and higher fecundity than queens living in associations of eight queens. As queens also differ neither in morphology nor the mode of colony foundation, our study shows that the social environment itself strongly affects ageing rate.     

Self-synchronization and task fulfilment in ant colonies

Some authors have hypothesized that the observed self-synchronized activity in ant colonies provides some adaptive advantages, and, in particular, it has been suggested that task realization may benefit from this ordered temporal pattern of behaviour (Robinson, 1992, Ann. Rev. Entomol, 37, 637-702; Hatcher et al., 1992, Naturwissenschaften, 79, 32-34). In this paper, we use a model of self-synchronized activity (the fluid neural network) to suggest that with self-synchronized patterns of activity a task may be fulfiled more effectively than with non-synchronized activity, at the same average level of activity per individual.     

Overdispersion of ant colonies: a test of hypotheses

Summary The nest locations of two ant species in the Colorado Desert are intraspecifically overdispersed. Intraspecific overdispersion has been thought to represent strong intraspecific competition. Here we consider this hypothesis along with three competing hypotheses: microhabitat selection by foundress queens, predation on foundress queens, and predation on established colonies. To test these hypotheses five types of data were collected: (1) the forager population sizes of Veromessor pergandei and Pogonomyrmex californicus, (2) the response of the territory use of V. pergandei to varying levels of food, (3) the encounter rates of conspecifics and other ant species to foundress queens artificially placed near and far from conspecific colonies, (4) predation on colonies as a function of colony spacing, and (5) the relationship between the plant microhabitat at the nest and colony spacing. The results show that established colonies have no apparent selectivity for a particular type of plant microhabitat nor do foundress queens show avoidance or attraction toward conspecifics. V. pergandei workers show only a slight ability to find V. pergandei queens that are artificially placed near their entrances. Certain spiders are the most common ant predators on our study area. Direct observations on spiders indicate that colonies with closer neighbors are not prone to a higher risk of predation. In addition, the estimates of the death rate of workers from a mark-recapture technique indicate that colonies with closer neighbors lose similar numbers of workers as compared to colonies with further neighbors. In favor of the competition hypothesis, the summed size of intraspecific nearest neighbor pairs are larger for colonies that are spaced further apart than those colonies that are spaced closer together. We also develop an index of foraging directionality for the column foraging species V. pergandei. Using this measure, we find that nearest neighbors tend to avoid foraging toward each other. The response of territory use to food levels was tested with experiments involving patches of cracked wheat. These experiments showed that patches away from nearest neighbors were found significantly sooner than patches toward nearest neighbors. The above five sets of data together suggest that resource competition and perhaps queen predation by established colonies account for the intraspecific spatial patterns of these species.     

Coupled oscillators and activity waves in ant colonies

We investigated the phenomenon of activity cycles in ants, taking into account the spatial structure of colonies. In our study species, Leptothorax acervorum, there are two spatially segregated groups in the nest. We developed a model that considers the two groups as coupled oscillators which can produce synchronized activity. By investigating the effects of noise on the model system we predicted how the return of foragers affects activity cycles in ant colonies. We tested these predictions empirically by comparing the activity of colonies under two conditions: when foragers are and are not allowed to return to the nest. The activity of the whole colony and of each group within the colony was studied using image analysis. This allowed us to reveal the spatial pattern of activity wave propagation in ant colonies for the first time.     

Social immunity and the evolution of group living in insects

The evolution of group living requires that individuals limit the inherent risks of parasite infection. To this end, group living insects have developed a unique capability of mounting collective anti-parasite defences, such as allogrooming and corpse removal from the nest. Over the last 20 years, this phenomenon (called social immunity) was mostly studied in eusocial insects, with results emphasizing its importance in derived social systems. However, the role of social immunity in the early evolution of group living remains unclear. Here, I investigate this topic by first presenting the definitions of social immunity and discussing their applications across social systems. I then provide an up-to-date appraisal of the collective and individual mechanisms of social immunity described in eusocial insects and show that they have counterparts in non-eusocial species and even solitary species. Finally, I review evidence demonstrating that the increased risks of parasite infection in group living species may both decrease and increase the level of personal immunity, and discuss how the expression of social immunity could drive these opposite effects. By highlighting similarities and differences of social immunity across social systems, this review emphasizes the potential importance of this phenomenon in the early evolution of the multiple forms of group living in insects.     

Genetic diversity promotes homeostasis in insect colonies

Although most insect colonies are headed by a singly mated queen, some ant, wasp and bee taxa have evolved high levels of multiple mating or 'polyandry'. We argue here that a contributing factor towards the evolution of polyandry is that the resulting genetic diversity within colonies provides them with a system of genetically based task specialization, enabling them to respond resiliently to environmental perturbation. An alternate view is that genetic contributions to task specialization are a side effect of multiple mating, which evolved through other causes, and that genetically based task specialization now makes little or no contribution to colony fitness.     

Random walk models of worker sorting in ant colonies

Sorting can be an important mechanism for the transfer of information from one level of biological organization to another. Here we study the algorithm underlying worker sorting in Leptothorax ant colonies. Worker sorting is related to task allocation and therefore to the adaptive advantages associated with an efficient system for the division of labour in ant colonies. We considered four spatially explicit individual-based models founded on two-dimensional correlated random walk. Our aim was to establish whether sorting at the level of the worker population could occur with minimal assumptions about the behavioural algorithm of individual workers. The behaviour of an individual worker in the models could be summarized by the rule "move if you can, turn always". We assume that the turning angle of a worker is individually specific and negatively dependent on the magnitude of an internal parameter micro which could be regarded as a measure of individual experience or task specialization. All four models attained a level of worker sortedness that was compatible with results from experiments onLeptothorax ant colonies. We found that the presence of a sorting pivot, such as the nest wall or an attraction force towards the centre of the worker population, was crucial for sorting. We make a distinction between such pivots and templates and discuss the biological implications of their difference.     

Reproductive specialization in multiple-queen colonies of the ant Formica exsecta

In polygynous (multiple queens per nest) colonies of socialinsects, queens can increase their reproductive share by layingmore eggs or by increasing the proportion of eggs that developinto reproductive individuals instead of workers. We used polymorphicmicrosatellite loci to determine the genetically effective contributionof queens to the production of gynes (new queens), males, and2 different cohorts of workers in a polygynous population ofthe ant Formica exsecta. For this purpose, we developed a newmethod that can be used for diploid and haplodiploid organismsto quantify the degree of reproductive specialization amongbreeders in societies where there are too many breeders to ascertainparentage. Using this method, we found a high degree of reproductivespecialization among nest-mate queens in both female- and male-producingcolonies (sex ratio is bimodally distributed in the study population).For example, a high effective proportion of queens (25% and79%, respectively) were specialized in the production of malesin female- and male-producing colonies. Our analyses furtherrevealed that in female-producing colonies, significantly fewerqueens contributed to gyne production than to worker production.Finally, we found significant changes in the identity of queenscontributing to different cohorts of workers. Altogether, thesedata demonstrate that colonies of F. exsecta, and probably thoseof many other highly polygynous social insect species, are composedof reproductive individuals differing in their investment togynes, males, and workers. These findings demonstrate a newaspect of the highly dynamic social organization of complexanimal societies.     

Economic investment by ant colonies in searches for better homes

Organisms should invest more in gathering information when the pay-off from finding a profitable resource is likely to be greater. Here, we ask whether animal societies put more effort in scouting for a new nest when their current one is of low quality. We measured the scouting behaviour of Temnothorax albipennis ant colonies when they inhabit nest-sites with different combinations of desirable attributes. We show that the average probability of an ant scouting decreases significantly with an increase in the quality of the nest in which the colony currently resides. This means that the greater the potential gain from finding a new nest, the more effort a colony puts into gathering information regarding new nest-sites. Our results show, for the first time to our knowledge, the ability of animal societies to respond collectively to the quality of a resource they currently have at their disposal (e.g. current nest-site) and regulate appropriately their information gathering efforts for finding an alternative (e.g. a potentially better nest-site).     

The regulation of foraging activity in red harvester ant colonies

Behavioral plasticity in social insects is intriguing because colonies adjust to environmental change through the aggregated responses of individuals. Without central control, colonies adjust numbers of workers allocated to various tasks. Individual decisions are based on local information from the environment and other workers. This study examines how colonies of the seed-eating ant Pogonomyrmex barbatus adjust the intensity of foraging in an arid environment where conspecific neighbors compete for foraging area. The main question is how foragers decide whether to leave the nest. Patrollers search the area before foragers emerge. Removal experiments show that the return of the patrollers stimulates the onset of foraging, and later, the rate at which foragers return affects the rate at which foragers continue to leave the nest. Foraging activity is less sensitive to changes in the rate of returning foragers than to changes in the rate of returning patrollers. These results suggest that whether a colony forages at all on a given day depends on conditions detected early by patrollers but that once foraging begins, the intensity of foraging does not track, on an hourly timescale, how quickly foragers can find food.