Social Insect Colonies Research Articles

Lazy workers are necessary for long-term sustainability in insect societies.

Optimality theory predicts the maximization of productivity in social insect colonies, but many inactive workers are found in ant colonies. Indeed, the low short-term productivity of ant colonies is often the consequence of high variation among workers in the threshold to respond to task-related stimuli. Why is such an inefficient strategy among colonies maintained by natural selection? Here, we show that inactive workers are necessary for the long-term sustainability of a colony. Our simulation shows that colonies with variable thresholds persist longer than those with invariable thresholds because inactive workers perform the critical function of replacing active workers when they become fatigued. Evidence of the replacement of active workers by inactive workers has been found in ant colonies. Thus, the presence of inactive workers increases the long-term persistence of the colony at the expense of decreasing short-term productivity. Inactive workers may represent a bet-hedging strategy in response to environmental stochasticity.

Highly specific responses to queen pheromone in three Lasius ant species

Queen pheromones mediate the reproductive division of labor in social insect colonies and provide novel opportunities for investigating the evolution of animal communication. Previous work found that queens in the ant genus Lasius produce several 3-methylalkanes in greater relative amounts than workers do. At least one of these (3-MeC31) is a queen pheromone that regulates worker sterility in two Lasius species, although there are indications that other 3-methylalkanes might also function as queen pheromones. Here, we presented workers from three Lasius species with four different 3-methylalkanes, and measured the effect on worker ovary development. In all three species, only 3-MeC31 showed clear evidence of inhibiting worker fecundity. Our results suggest that worker ants can discriminate homologous hydrocarbons that differ in chain length and only treat specific homologs as queen pheromones. These results provide insight into the conflicting selective pressures on cuticular hydrocarbons arising from their multiple roles in signaling and adaptation to the abiotic environment.

Colony pace: a life-history trait affecting social insect epidemiology.

Among colonies of social insects, the worker turnover rate (colony 'pace') typically shows considerable variation. This has epidemiological consequences for parasites, because in 'fast-paced' colonies, with short-lived workers, the time of parasite residence in a given host will be reduced, and further transmission may thus get less likely. Here, we test this idea and ask whether pace is a life-history strategy against infectious parasites. We infected bumblebees (Bombus terrestris) with the infectious gut parasite Crithidia bombi, and experimentally manipulated birth and death rates to mimic slow and fast pace. We found that fewer workers and, importantly, fewer last-generation workers that are responsible for rearing sexuals were infected in colonies with faster pace. This translates into increased fitness in fast-paced colonies, as daughter queens exposed to fewer infected workers in the nest are less likely to become infected themselves, and have a higher chance of founding their own colonies in the next year. High worker turnover rate can thus act as a strategy of defence against a spreading infection in social insect colonies.

From division of labor to the collective behavior of social insects

‘Division of labor’ is a misleading way to describe the organization of tasks in social insect colonies, because there is little evidence for persistent individual specialization in task. Instead, task allocation in social insects occurs through distributed processes whose advantages, such as resilience, differ from those of division of labor, which are mostly based on learning. The use of the phrase ‘division of labor’ persists for historical reasons, and tends to focus attention on differences among individuals in internal attributes. This focus distracts from the main questions of interest in current research, which require an understanding of how individuals interact with each other and their environments. These questions include how colony behavior is regulated, how the regulation of colony behavior develops over the lifetime of a colony, what are the sources of variation among colonies in the regulation of behavior, and how the collective regulation of colony behavior evolves.

Ant larvae regulate worker foraging behavior and ovarian activity in a dose-dependent manner.

Division of labor in insect societies relies on simple behavioral rules, whereby individual colony members respond to dynamic signals indicating the need for certain tasks to be performed. This in turn gives rise to colony-level phenotypes. However, empirical studies quantifying colony-level signal-response dynamics are lacking. Here, we make use of the unusual biology and experimental amenability of the queenless clonal raider ant Cerapachys biroi, to jointly quantify the behavioral and physiological responses of workers to a social signal emitted by larvae. Using automated behavioral quantification and oocyte size measurements in colonies of different sizes and with different worker to larvae ratios, we show that the workers in a colony respond to larvae by increasing foraging activity and inhibiting ovarian activation in a progressive manner, and that these responses are stronger in smaller colonies. This work adds to our knowledge of the processes that link plastic individual behavioral/physiological responses to colony-level phenotypes in social insect colonies.

Differentiated Anti-Predation Responses in a Superorganism.

Insect societies are complex systems, displaying emergent properties much greater than the sum of their individual parts. As such, the concept of these societies as single ‘superorganisms’ is widely applied to describe their organisation and biology. Here, we test the applicability of this concept to the response of social insect colonies to predation during a vulnerable period of their life history. We used the model system of house-hunting behaviour in the ant Temnothorax albipennis. We show that removing individuals from directly within the nest causes an evacuation response, while removing ants at the periphery of scouting activity causes the colony to withdraw back into the nest. This suggests that colonies react differentially, but in a coordinated fashion, to these differing types of predation. Our findings lend support to the superorganism concept, as the whole society reacts much like a single organism would in response to attacks on different parts of its body. The implication of this is that a collective reaction to the location of worker loss within insect colonies is key to avoiding further harm, much in the same way that the nervous systems of individuals facilitate the avoidance of localised damage.

Interactions Increase Forager Availability and Activity in Harvester Ants

Social insect colonies use interactions among workers to regulate collective behavior. Harvester ant foragers interact in a chamber just inside the nest entrance, here called the 'entrance chamber'. Previous studies of the activation of foragers in red harvester ants show that an outgoing forager inside the nest experiences an increase in brief antennal contacts before it leaves the nest to forage. Here we compare the interaction rate experienced by foragers that left the nest and ants that did not. We found that ants in the entrance chamber that leave the nest to forage experienced more interactions than ants that descend to the deeper nest without foraging. Additionally, we found that the availability of foragers in the entrance chamber is associated with the rate of forager return. An increase in the rate of forager return leads to an increase in the rate at which ants descend to the deeper nest, which then stimulates more ants to ascend into the entrance chamber. Thus a higher rate of forager return leads to more available foragers in the entrance chamber. The highest density of interactions occurs near the nest entrance and the entrances of the tunnels from the entrance chamber to the deeper nest. Local interactions with returning foragers regulate both the activation of waiting foragers and the number of foragers available to be activated.

Queen Killing Is Linked to High Worker-Worker Relatedness in a Social Wasp

Social insect colonies are pinnacles of evolved altruism but also exhibit dramatic conflict among relatives. In many species, a colony's workers compete with the queen and each other over the production of males. Interspecific comparisons demonstrate the importance of within-colony relatedness in determining the outcome of such conflicts, but facultative responses to within-colony relatedness are rarely reported. Here, I report facultative matricide (worker killing of a colony's queen) in the social wasp Dolichovespula arenaria. Matricide is strongly associated with high worker-worker relatedness, as predicted by theory, because closely related workers value nephews more than brothers. This pattern is the result of variation in both paternity frequency and the paternity skew of colonies with multiple patrilines, implicating worker-worker relatedness rather than a direct effect of multiple mating on queen survival. Furthermore, occasional inbreeding can explain why some multiple-patriline colonies exhibit high paternity skew associated with matricide. In general, these results support the hypothesis that workers can facultatively respond to intracolony relatedness determined by queen mating behavior and demonstrate a novel benefit of polyandry in annual social insects. Facultative matricide shows dramatically how workers are evolutionary actors with interests that can diverge from the queen's, rather than being "extrasomatic projections of her personal genome".

Effect of Pair Interactions on Transition Probabilities between Inactive and Active States — Achieving Collective Behaviour via Pair Interactions in Social Insects —

To understand the evolution of well-organized social behaviour, we must first understand the mechanism by which collective behaviour is established. In this study, the mechanisms of collective behaviour in a colony of social insects were studied in terms of the transition probability between active and inactive states, which is linked to mutual interactions. The active and inactive states of the social insects were statistically extracted from the velocity profiles. From the duration distributions of the two states, we found that (1) the durations of active and inactive states follow an exponential law, and (2) pair interactions increase the transition probability from inactive to active states. The regulation of the transition probability by pair interactions suggests that such interactions control the populations of active and inactive workers in the colony.

Parasites modulate within-colony activity and accelerate the temporal polyethism schedule of a social insect, the honey bee.

Task allocation in social insect colonies is generally organised into an age-related division of labour, termed the temporal polyethism schedule, which may in part have evolved to reduce infection of the colony’s brood by pests and pathogens. The temporal polyethism schedule is sensitive to colony perturbations that may lead to adaptive changes in task allocation, maintaining colony homeostasis. Though social insects can be infected by a range of parasites, little is known of how these parasites impact within-colony behaviour and the temporal polyethism schedule. We use honey bees (Apis mellifera) experimentally infected by two of their emerging pathogens, Deformed wing virus (DWV), which is relatively understudied concerning its behavioural impact on its host, and the exotic microsporidian Nosema ceranae. We examined parasite effects on host temporal polyethism and patterns of activity within the colony. We found that pathogens accelerated the temporal polyethism schedule, but without reducing host behavioural repertoire. Infected hosts exhibited increased hyperactivity, allocating more time to self-grooming and foraging-related tasks. The strength of behavioural alterations we observed was found to be pathogen specific; behavioural modifications were more pronounced in virus-treated hosts versus N. ceranae-treated hosts, with potential benefits for the colony in terms of reducing within-colony transmission. Investigating the effects of multiple pathogens on behavioural patterns of social insects could play a crucial role in understanding pathogen spread within a colony and their effects on colony social organisation.Electronic supplementary materialThe online version of this article (doi:10.1007/s00265-015-2019-5) contains supplementary material, which is available to authorized users.

Ant recognition cue diversity is higher in the presence of slavemaker ants

Social insect colonies defend themselves from intruders through nestmate recognition, yet the evolution and maintenance of recognition cue diversity is still poorly understood. We compared the recognition cue diversity of 9 populations of Temnothorax longispinosus ant colonies, including populations that harbored the socially parasitic slavemaker ant, Protomognathus americanus. Although ants recognize friends from foe based on recognition cues encoded in their cuticular hydrocarbon profile, which specific compounds are involved in recognition is unknown for most species. We therefore started by statistically identifying 9 putative recognition compounds involved in worker and colony aggression. We find that colonies that co-occur with slavemakers were more variable in these recognition compounds and hence less similar in their recognition profiles than unparasitized populations. Importantly, these differences appear to be regulated by processes that specifically act on the level of the colony, which rules out potentially confounding effects altering chemical profiles of populations, such as differences in abiotic conditions or standing genetic variation. Instead, our findings indicate that slavemakers drive recognition cue diversity in their ant hosts, in much the same way that avian hosts diversify their egg appearance in response to brood parasite pressure. Such recognition cue diversification through negative frequency-dependent selection favors rare host phenotypes and renders it impossible for parasites to match the recognition profile of all potential hosts.

Ant Colonies Do Not Trade-Off Reproduction against Maintenance.

The question on how individuals allocate resources into maintenance and reproduction is one of the central questions in life history theory. Yet, resource allocation into maintenance on the organismic level can only be measured indirectly. This is different in a social insect colony, a “superorganism” where workers represent the soma and the queen the germ line of the colony. Here, we investigate whether trade-offs exist between maintenance and reproduction on two levels of biological organization, queens and colonies, by following single-queen colonies of the ant Cardiocondyla obscurior throughout the entire lifespan of the queen. Our results show that maintenance and reproduction are positively correlated on the colony level, and we confirm results of an earlier study that found no trade-off on the individual (queen) level. We attribute this unexpected outcome to the existence of a positive feedback loop where investment into maintenance (workers) increases the rate of resource acquisition under laboratory conditions. Even though food was provided ad libitum, variation in productivity among the colonies suggests that resources can only be utilized and invested into additional maintenance and reproduction by the colony if enough workers are available. The resulting relationship between per-capita and colony productivity in our study fits well with other studies conducted in the field, where decreasing per-capita productivity and the leveling off of colony productivity have been linked to density dependent effects due to competition among colonies. This suggests that the absence of trade-offs in our laboratory study might also be prevalent under natural conditions, leading to a positive association of maintenance, (= growth) and reproduction. In this respect, insect colonies resemble indeterminate growing organisms.

Social Biomimicry: what do ants and bees tell us about organization in the natural world?

The social insects serve as exemplars for social biomimicry, the search for social design inspiration from the natural world. Although their group members are individually much simpler than humans, social insect colonies provide elegant tutorials on the large-scale outcomes that can be achieved by social interactions and self-organizational processes. These range from complex physical structures built by collective effort; to exemplars of flexible work organization; to effective consensus building in group decisions. This special issue highlights examples of the lessons to be learned from the bees and ants, providing ways to think about how humans can (and in some cases should not) borrow from social insect rules of organization and their collective outcomes.

When doing nothing is something. How task allocation strategies compromise between flexibility, efficiency, and inactive agents

We expect that human organizations and cooperative animal groups should be optimized for collective performance. This often involves the allocation of different individuals to different tasks. Social insect colonies are a prime example of cooperative animal groups that display sophisticated mechanisms of task allocation. Here we discuss which task allocation strategies may be adapted to which environmental and social conditions. Effective and robust task allocation is a hard problem, and in many biological and engineered complex systems is solved in a decentralized manner: human organizations may benefit from insights into what makes decentralized strategies of group organization effective. In addition, we often find considerable variation among individuals in how much work they appear to contribute, despite the fact that individual selfishness in social insects is low and optimization occurs largely at the group level. We review possible explanations for uneven workloads among workers, including limitations on individual information collection or constraints of task allocation efficiency, such as when there is a mismatch between the frequency of fluctuations in demand for work and the speed at which workers can be reallocated. These processes are likely to apply to any system in which worker agents are allocated to tasks with fluctuating demand, and should therefore be instructive to understanding optimal task allocation and inactive workers in any distributed system. Some of these processes imply that a certain proportion of inactive workers can be an adaptive strategy for collective organization.

Intraspecific Variation among Social Insect Colonies: Persistent Regional and Colony-Level Differences in Fire Ant Foraging Behavior.

Individuals vary within a species in many ecologically important ways, but the causes and consequences of such variation are often poorly understood. Foraging behavior is among the most profitable and risky activities in which organisms engage and is expected to be under strong selection. Among social insects there is evidence that within-colony variation in traits such as foraging behavior can increase colony fitness, but variation between colonies and the potential consequences of such variation are poorly documented. In this study, we tested natural populations of the red imported fire ant, Solenopsis invicta, for the existence of colony and regional variation in foraging behavior and tested the persistence of this variation over time and across foraging habitats. We also reared single-lineage colonies in standardized environments to explore the contribution of colony lineage. Fire ants from natural populations exhibited significant and persistent colony and regional-level variation in foraging behaviors such as extra-nest activity, exploration, and discovery of and recruitment to resources. Moreover, colony-level variation in extra-nest activity was significantly correlated with colony growth, suggesting that this variation has fitness consequences. Lineage of the colony had a significant effect on extra-nest activity and exploratory activity and explained approximately half of the variation observed in foraging behaviors, suggesting a heritable component to colony-level variation in behavior.

Reproductive physiology mediates honey bee (Apis mellifera) worker responses to social cues

Though social insect colonies are often considered to be models of cooperative behavior, there can be conflict between queens and their workers over reproduction. In honey bees (Apis mellifera), the queen releases a pheromone that attracts workers and inhibits worker ovary activation such that they remain sterile and rear the offspring of the queen. Furthermore, under queenless conditions, workers can rear new queens from the old queen’s eggs or activate their ovaries and lay their own eggs. Workers vary greatly in their ability to activate their ovaries, and this variation is positively correlated with ovary size. Here, we demonstrate that, compared to their sisters, workers with the larger ovaries are less attracted to queen pheromone, less likely to rear new queens if the old queen is lost, and more likely to activate their ovaries in the absence of a queen. Furthermore, surgically increasing a bee’s ovarian mass reduces her attraction to queen pheromone. The additional ovarian mass altered brain expression levels of the octopamine receptor, Oa1, but these differences did not correlate with response to queen pheromone. Overall, these results indicate that honey bee workers’ response to social cues under both queenright and queenless contexts is modified by their reproductive physiology, such that workers with greater ovary activation rates are less likely to engage in behaviors that promote the queen’s reproduction.

Patriline Differences Reveal Genetic Influence on Forewing Size and Shape in a Yellowjacket Wasp (Hymenoptera: Vespidae: Vespula flavopilosa Jacobson, 1978).

The wing venation is frequently used as a morphological marker to distinguish biological groups among insects. With geometric morphometrics, minute shape differences can be detected between closely related species or populations, making this technique useful for taxonomy. However, the direct influence of genetic differences on wing morphology has not been explored within colonies of social insects. Here, we show that the father’s genotype has a direct effect on wing morphology in colonies of social wasps. Using geometric morphometrics on the venation pattern, we found significant differences in wing size and shape between patrilines of yellowjackets, taking allometry and measurement error into account. The genetic influence on wing size accounted for a small part of the overall size variation, but venation shape was highly structured by the differences between patrilines. Overall, our results showed a strong genetic influence on wing morphology likely acting at multiple levels of venation pattern development. This confirmed the pertinence of this marker for taxonomic purposes and suggests this phenotype as a potentially useful marker for phylogenies. This also raises doubts about the strength of selective pressures on this phenotype, which highlights the need to understand better the role of wing venation shape in insect flight.

Workers ‘specialized’ on inactivity: Behavioral consistency of inactive workers and their role in task allocation

Social insect colonies are often considered to be highly efficient collective systems, with division of labor at therootoftheirecologicalsuccess.However,inmanyspecies, a large proportion of a colony's workers appear to spend their time completely inactive. The role of this inactivity for colony function remains unclear. Here, we investigate how inactivity is distributed among workers and over time in the ant Temnothorax rugatulus. We show that the level of inactivity is consistent for individual workers, but differs significantly among workers, that is, some workers effectively specialize on 'inactivity'. We also show that workers have circadian rhythms, although intra-nest tasks tend to be performed uni- formly across the whole day. Differences in circadian rhythms, or workers taking turns resting (i.e., working in shifts), cannot explain the observation that some workers are consistently inactive. Using extensive individual-level data to describe the overall structure of division of labor, we show that 'inactive workers' form a group distinct from other task groups. Hierarchical clustering suggests that inactivity is the primaryvariableindifferentiatingbothworkersandtasks.Our results underline the importance of inactivity as a behavioral state and the need for further studies on its evolution.

Does altruism exist?: culture, genes, and the welfare of others

Does altruism exist? Or is human nature entirely selfish? In this eloquent and accessible book, famed biologist David Sloan Wilson provides new answers to this age-old question based on the latest developments in evolutionary science. From an evolutionary viewpoint, Wilson argues, altruism is inextricably linked to the functional organization of groups. Groups that work undeniably exist in nature and human society, although special conditions are required for their evolution. Humans are one of the most groupish species on earth, in some ways comparable to social insect colonies and multi-cellular organisms. The case that altruism evolves in all social species is surprisingly simple to make. Yet the implications for human society are far from obvious. Some of the most venerable criteria for defining altruism aren't worth caring much about, any more than we care much whether we are paid by cash or check. Altruism defined in terms of thoughts and feelings is notably absent from religion, even though altruism defined in terms of action is notably present. The economic case for selfishness can be decisively rejected. The quality of everyday life depends critically on people who overtly care about the welfare of others. Yet, like any other adaptation, altruism can have pathological manifestations. Wilson concludes by showing how a social theory that goes beyond altruism by focusing on group function can help to improve the human condition.

Rapid increase of the parasitic fungus Laboulbenia formicarum in supercolonies of the invasive garden ant Lasius neglectus

A key feature among invasive ant species is their ability to dominate vast areas by forming dense networks of connected nests in contrast to the smaller and discrete, spatially dispersed colonies of most social insects. However, it was recently proposed that such supercolonies are more vulnerable to infection by parasites and diseases as they would serve as large targets with high rates of transmission from nests to nest. We studied the invasive garden ant Lasius neglectus, a pest species currently spreading throughout Europe. Several populations are infected with an ectoparasitic fungus, Laboulbenia formicarum, itself an introduced species, yielding a new host–parasite relationship. Long-term monitoring of the prevalence and intensity of infection in two populations (supercolonies) over 4–10 years revealed epizootic spread of the parasite with a 14 % annual increase in prevalence until ca. 80 % of all ants were infected. In contrast, no other local ant species with discrete colonies carried the parasite, although a local species (Lasius niger) proved susceptible in a cross-infection experiment. These results support the hypothesis that supercolonies potentially face an important challenge from parasites and diseases, with interesting perspectives for biological control of such ant species.