Social Insect Colonies Research Articles

Recruitment Dynamics of Social Insect Colonies

Recruitment plays a vital role in the ecological and evolutionary successes of social insect colonies. In this paper, we formulate a four-compartment model and its simplified version to explore how...

Intransitivity and Contextuality in the Decision Making of Social Insect Colonies

Intransitivity and Contextuality in the Decision Making of Social Insect Colonies

Macroevolutionary integration of phenotypes within and across ant worker castes.

Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies, the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genus Pheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus, Pheidole workers are evolving as a mixture of intracaste and intercaste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.

Nutritional regulation influencing colony dynamics and task allocations in social insect colonies

In this paper, we use an adaptive modeling framework to model and study how nutritional status (measured by the protein to carbohydrate ratio) may regulate population dynamics and foraging task allocation of social insect colonies. Mathematical analysis of our model shows that both investment to brood rearing and brood nutrition are important for colony survival and dynamics. When division of labour and/or nutrition are in an intermediate value range, the model undergoes a backward bifurcation and creates multiple attractors due to bistability. This bistability implies that there is a threshold population size required for colony survival. When the investment in brood is large enough or nutritional requirements are less strict, the colony tends to survive, otherwise the colony faces collapse. Our model suggests that the needs of colony survival are shaped by the brood survival probability, which requires good nutritional status. As a consequence, better nutritional status can lead to a better survival rate of larvae and thus a larger worker population.

Superorganism Immunity: A Major Transition in Immune System Evolution

Social insect colonies can express adaptive, organism-like design. In some cases, colonies so resemble a unique, cohesive and integrated “individual” that they are termed superorganisms. The major evolutionary transitions framework explains, via inclusive fitness theory, how new levels of biological individuality, including genes into genomes within cells, cells into multicellular organisms and organisms into superorganisms can emerge. Importantly, it highlights how at each major transition similar challenges arose and why seemingly convergent solutions evolved. One challenge faced at each transition is exploitation, caused internally by social cheaters, and externally by parasites and pathogens. To overcome the problem of exploitation transitions in biological individuality required novel immune systems to maintain the integrity of newly emerged individuals. Multicellular organisms evolved an immune system while social insect colonies evolved a social immune system. In this review, we take a major transitions perspective of immunity to highlight the interdependency between the evolution of immune systems and the emergence of biological individuality. We build on the notion that superorganisms have evolved an immune system to promote the fitness of the colony. We draw parallels between the evolution of the metazoan immune system and the social immune system, and their expression as cognitive networks. Moreover, we discuss how research on other group-living species, such as family-based cooperative breeders, can inform our understanding of how social immune systems evolve. We conclude that “superorganism immunity” is an adaptive suite of organismal traits that evolves to maximise the fitness of advanced social insect colonies, fulfilling the same function as the immune system of Metazoa.

Evolutionarily stable investments in recognition systems explain patterns of discrimination failure and success.

Many animals are able to perform recognition feats that astound us-such as a rodent recognizing kin it has never met. Yet in other contexts, animals appear clueless as when reed warblers rear cuckoo chicks that bear no resemblance to their own species. Failures of recognition when it would seem adaptive have been especially puzzling. Here, we present a simple tug-of-war game theory model examining how individuals should optimally invest in affecting the accuracy of discrimination between desirable and undesirable recipients. In the game, discriminating individuals (operators) and desirable and undesirable recipients (targets and mimics, respectively) can all invest effort into their own preferred outcome. We demonstrate that stable inaccurate recognition will arise when undesirable recipients have large fitness gains from inaccurate recognition relative to the pay-offs that the other two parties receive from accurate recognition. The probability of accurate recognition is often determined by just the relative pay-offs to the desirable and undesirable recipients, rather than to the discriminator. Our results provide a new lens on long-standing puzzles including a lack of nepotism in social insect colonies, tolerance of brood parasites and male birds caring for extra-pair young in their nests, which our model suggests should often lack accurate discrimination. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Task partitioning in ants lacking discrete morphological worker subcastes

Task partitioning allows for efficient coordination of behavior in social insect colonies. Many task allocation studies focus on social insect species with discrete morphological worker subcastes, such as those possessing major and minor workers with strongly differentiated body plans. Much less is known about task partitioning among size-variable workers lacking discrete morphological subcastes. We investigated task fidelity and its correlation with worker size in Formica species with differing degrees of body size variation. During a mark-recapture study that focused on three worker tasks (honeydew collection, nest building, and protein foraging) across 2 days, 98.6% of 3570 recaptured workers exhibited task fidelity. In species with high levels of worker size variation, worker size is strongly correlated with task performance. This size-task correlation is weaker, but still present, in species with less variably sized workers. Our results suggest that Formica use size-based task partitioning, a form of morphological polyethism. We expect social insects with and without discrete morphological worker subcastes to differ in ontogeny, evolutionary history, and degree of behavioral flexibility. Identifying the scope of variation in task partitioning mechanisms will facilitate comparative studies, thereby elucidating evolutionary histories and outcomes of alternative strategies. Division of labor is thought to increase the efficiency and success of animal societies by allowing the performance of multiple tasks in parallel, rather than sequentially. We investigated the task partitioning strategy employed by an ecologically dominant ant genus characterized by continuous worker size variation but lacking discrete morphological worker subcastes. We show that several species employ a form of morphological polyethism, wherein individuals specialize in tasks according to body size. Size-mediated morphological polyethism in the absence of discrete morphological worker subcastes has been demonstrated in a few other social insects. However, this task allocation strategy is likely more common than previously recognized, as most insect societies display natural worker size variation. Further, we argue that it is important to distinguish between size- and subcaste-based morphological polyethism. Alternative task partitioning strategies are likely to impact animal societies’ resilience to environmental perturbations, which are becoming increasingly common in the face of global change.

High numbers of unrelated reproductives in the Australian ‘higher’ termite Nasutitermes exitiosus (Blattodea: Termitidae)

Social insect colonies are among the most complex social organisations in nature, with reproductive and non-reproductive individuals co-ordinating to maintain the survival of the colony. Multiple reproductive schemes occur in social insects, from simple schemes with one founding reproductive pair, to more complex ones involving within-colony inbreeding and more than two unrelated reproductives. Colony breeding schemes and genetic structure remain understudied in termites, compared to the Hymenoptera. In this study, we performed the first genetic characterisation of the colony breeding structure of Nasutitermes exitiosus (Blattodea: Termitidae), an endemic Australian termite with a broad distribution across southern mainland Australia. We analysed the genetic structure of 60 N. exitiosus colonies from the Eastern part of its distribution, using microsatellites and mitochondrial sequence data. We found that most colonies were headed by one founding pair of reproductives, although some colonies exhibited a more complex breeding structure, including within-colony inbreeding and the presence of multiple unrelated reproductives. We found evidence for the presence of seven unrelated queens in one colony, to our knowledge, the highest number of unrelated queens yet found in a termite from the family Termitidae. We found some evidence for genetic isolation by distance, indicating that the species is a relatively poor disperser over long ranges.

Colony Volatiles and Substrate-borne Vibrations Entrain Circadian Rhythms and Are Potential Cues Mediating Social Synchronization in Honey Bee Colonies.

Internal circadian clocks organize animal behavior and physiology and are entrained by ecologically relevant external time-givers such as light and temperature cycles. In the highly social honey bee, social time-givers are potent and can override photic entrainment, but the cues mediating social entrainment are unknown. Here, we tested whether substrate-borne vibrations and hive volatiles can mediate social synchronization in honey bees. We first placed newly emerged worker bees on the same or on a different substrate on which we placed cages with foragers entrained to ambient day-night cycles, while minimizing the spread of volatiles between cages. In the second experiment, we exposed young bees to constant airflow drawn from either a free-foraging colony or a similar-size control hive containing only heated empty honeycombs, while minimizing transfer of substrate-borne vibrations between cages. After 6 days, we isolated each focal bee in an individual cage in an environmental chamber and monitored her locomotor activity. We repeated each experiment 5 times, each trial with bees from a different source colony, monitoring a total of more than 1000 bees representing diverse genotypes. We found that bees placed on the same substrate as foragers showed a stronger phase coherence and a phase more similar to that of foragers compared with bees placed on a different substrate. In the second experiment, bees exposed to air drawn from a colony showed a stronger phase coherence and a phase more similar to that of foragers compared with bees exposed to air from an empty hive. These findings lend credence to the hypothesis that surrogates of activity entrain circadian rhythms and suggest that multiple social cues can act in concert to entrain social insect colonies to a common phase.

Comparative study of population genomic approaches for mapping colony-level traits.

Social insect colonies exhibit colony-level phenotypes such as social immunity and task coordination, which are produced by the individual phenotypes. Mapping the genetic basis of such phenotypes requires associating the colony-level phenotype with the genotypes in the colony. In this paper, we examine alternative approaches to DNA extraction, library construction, and sequencing for genome wide association studies (GWAS) of colony-level traits using a population sample of Cataglyphis niger ants. We evaluate the accuracy of allele frequency estimation from sequencing a pool of individuals (pool-seq) from each colony using either whole-genome sequencing or reduced representation genomic sequencing. Based on empirical measurement of the experimental noise in sequenced DNA pools, we show that reduced representation pool-seq is drastically less accurate than whole-genome pool-seq. Surprisingly, normalized pooling of samples did not result in greater accuracy than un-normalized pooling. Subsequently, we evaluate the power of the alternative approaches for detecting quantitative trait loci (QTL) of colony-level traits by using simulations that account for an environmental effect on the phenotype. Our results can inform experimental designs and enable optimizing the power of GWAS depending on budget, availability of samples and research goals. We conclude that for a given budget, sequencing un-normalized pools of individuals from each colony provides optimal QTL detection power.

Tissue Specificity in Social Context-Dependent lysozyme Expression in Bumblebees.

Group living at high densities may result in the enhanced transmission of pathogens. Social insects are obligate group-living species, which often also exhibit high relatedness and frequent social interactions amongst individuals, resulting in a high risk of disease spread. Social species seem to exhibit immune systems that provide colonies of social insects with a certain level of flexibility for adjustment of immune activity according to the risk of disease spread. In bumblebees, Bombus terrestris, it was demonstrated that in group-kept individuals, immune component activity and immune gene expression is increased, potentially as a prophylactic adaptation. Here, I tested whether social environment influences the gene expression pattern of two lysozyme genes, which are components of the antimicrobial response of the bumblebee. In addition, I tested gene expression activation in different tissues (gut, fat body). The analysis revealed that the gene, the density of individuals, the tissue, and the interaction of the latter are the main factors that influence the expression of lysozyme genes. This is the first report of a tissue-specific response towards the social environment. This has implications for gene regulation, which must be responsive to social context-dependent information.

Dynamics of social interactions, in the flow of information and disease spreading in social insects colonies: Effects of environmental events and spatial heterogeneity

The relationship between division of labor and individuals’ spatial behavior in social insect colonies provides a useful context to study how social interactions influence the spreading of elements (which could be information, virus or food) across distributed agent systems. In social insect colonies, spatial heterogeneity associated with variations of individual task roles, affects social contacts, and thus the way in which agent moves through social contact networks. We used an Agent Based Model (ABM) to mimic three realistic scenarios of elements’ transmission, such as information, food or pathogens, via physical contact in social insect colonies. Our model suggests that individuals within a specific task interact more with consequences that elements could potentially spread rapidly within that group, while elements spread slower between task groups. Our simulations show a strong linear relationship between the degree of spatial heterogeneity and social contact rates, and that the spreading dynamics of elements follow a modified nonlinear logistic growth model with varied transmission rates for different scenarios. Our work provides important insights on the dual-functionality of physical contacts. This dual-functionality is often driven via variations of individual spatial behavior, and can have both inhibiting and facilitating effects on elements’ transmission rates depending on environment. The results from our proposed model not only provide important insights on mechanisms that generate spatial heterogeneity, but also deepen our understanding of how social insect colonies balance the benefit and cost of physical contacts on the elements’ transmission under varied environmental conditions.

Behavioral responses to colony-level properties affect disturbance resistance of red harvester ant colonies

Self-organizing biological systems, such as colonies of social insects, are characterized by their decentralized control and flexible responses to changing environments, often likened to swarm intelligence. Although decentralized control is well known to be a product of local interactions among agents, without the need for a bird’s-eye view, indirect knowledge of properties that indicate the current states of the entire system also helps each agent to respond to changes, thereby leading to a more adaptive system. In this study, we analyze the rules that govern workers’ behavioral responses to colony-level properties and assess whether they contribute to adaptive flexibility in social insect colonies. We focus on task allocation among red harvester ants (Pogonomyrmex barbatus) as a model system and develop an ordinary differential equation model to describe the system of task allocation among workers. We simulate 12 scenarios specifying how workers respond to changes in the colony-level properties of colony size and nutritional state. We found that when workers decrease their contact rates in response to increasing colony size, they enable achievement of a larger colony size, similar to that of P. barbatus colonies in nature, and when workers increase their foraging levels in response to decreasing colony-wide nutritional levels, they increase resilience to environmental disturbances. These negative feedback rules governing the response to colony-level properties are consistent with previous reports on ants and honeybees.

Comparative advantage and caste evolution.

Most of the theory for the evolution of caste specialization in social insects assumes that increased efficiency in worker labor leads to specialization and increased worker efficiency gives colonies with behavioral specialists an advantage. However, there are an increasing number of studies that show that the task specialists within social insect colonies do not have the highest efficiency. Indeed, some studies show that some groups of workers are uniformly better than all other groups at every task. In this note, I adapt the principle of comparative advantage from economics to show that, rather than maximizing the payoff, specialization is advantageous when minimizing opportunity costs. This leads to the prediction that caste specialization should be associated with reduced opportunity costs rather than increased task efficiency.

Evolutionary conflict and coloniality in animals.

Despite considerable interest in the effects of evolutionary conflict in colonies of social insects, relatively little attention has been paid to this issue in clonal animals with modular construction, such as colonial ascidians, bryozoans, and cnidarians. These colonial animals are structural individuals, subdivided into repeated morphological modules, which can individually acquire, process, and share resources. While size-related selection favors colony formation, evolutionary conflicts remain a potent obstacle to such cooperation. These conflicts can occur at several levels and must be mediated for cooperation to emerge. Module-level conflicts potentially result in coalitions of genetically similar modules failing to share resources or monopolizing reproduction. Mediation occurs by a number of mechanisms including: (a) a single-module bottleneck at the initiation of colony formation, (b) allorecognition that limits colony fusion to close kin, (c) development of new modules from connective tissue, (d) synchronization of module budding, (e) programmed module death, (f) terminal differentiation of reproductive modules, and (g) architectural constraints. Effective mediation of module-level conflicts, however, may in some cases contribute to cell-level conflicts. Animal colonies typically have multipotent stem cells, and genetically variant stem cells can potentially monopolize gamete formation. Limiting colony fusion to close kin may not eliminate such conflict. Finally, in at least some taxa an association between photosymbiosis and coloniality is found. Allocation of photosynthate can lead to host-symbiont conflicts that can be mediated by housing symbionts intracellularly and using chemiosmotic mechanisms to detect defectors. Colonial animals thus serve as a living laboratory of evolutionary conflict and its mediation.

Synergies Between Division of Labor and Gut Microbiomes of Social Insects

Social insects maximize resource acquisition and allocation through division of labor and associations with microbial symbionts. Colonies divide labor among castes and subcastes, where the plasticity of caste roles decreases in clades with higher social grades. Recent studies indicate that specific castes may also foster distinct gut microbiomes, suggesting synergies between division of labor and symbiosis. The social organization of a colony potentially partitions evolutionary persistent microbial partners to optimize symbioses and complement division of labor. However, research in this area has received limited attention. To elucidate if a structured microbiota is adaptive, we present three testable predictions to address consistent community structure, beneficial functions, and selection for microbiota that support caste roles. First, we posit that social insect groups spanning lower to higher social grades exhibit increasingly distinct caste microbiomes, suggesting that structured microbiomes may have evolved in parallel to social complexity. Second, we contend that the development of these microbiomes during colony maturation may clarify the extent to which they support division of labor. Third, we predict that mature social insect colonies with the most extreme division of labor demonstrate the strongest distinctions between caste microbiomes, carrying the greatest promise of insight into microbiome composition and function. Ultimately, we hypothesize that caste-specific microbiomes may enhance symbiotic benefits and the efficiency of division of labor, consequently maximizing fitness.

Lipid content influences division of labour in a clonal ant.

The fat body, a major metabolic hub in insects, is involved in many functions, e.g. energy storage, nutrient sensing and immune response. In social insects, fat appears to play an additional role in division of labour between egg layers and workers, which specialize in non-reproductive tasks inside and outside their nest. For instance, reproductives are more resistant to starvation, and changes in fat content have been associated with the transition from inside to outside work or reproductive activities. However, most studies have been correlative and we still need to unravel the causal interrelationships between fat content and division of both reproductive and non-reproductive labour. Clonal ants, e.g. Platythyrea punctata, are ideal models for studying task partitioning without confounding variation in genotype and morphology. In this study, we examined the range of variation and flexibility of fat content throughout the lifespan of workers, the threshold of corpulence associated with foraging or reproduction and whether low fat content is a cause rather than a consequence of the transition to foraging. We found that lipid stores change with division of labour from corpulent to lean and, in reverted nurses, back to corpulent. In addition, our data show the presence of fat content thresholds that trigger the onset of foraging or egg-laying behaviour. Our study supports the view that mechanisms that regulate reproduction and foraging in solitary insects, in particular the nutritional status of individuals, have been co-opted to regulate division of labour in colonies of social insects.

Circadian rhythms and clock in the colony of social insects.

Circadian rhythms and clock in the colony of social insects.

Controlling invasive Argentine ants, Linepithema humile, in conservation areas using horizontal insecticide transfer

Invasive ants are major agricultural and urban pests and a significant concern in conservation areas. Despite long history of control and eradication efforts, invasive ants continue to spread around the globe driven by a multitude of synergistic factors. Lack of effective management tools is one of the biggest challenges in controlling invasive ants. The goal of the current study was to improve the efficacy and safety of ant management and to develop effective control strategies for sensitive conservation areas. We utilized the Argentine ant (Linepithema humile) as a model system to evaluate a target-specific pesticide delivery system that exploits the interconnected nature of social insect colonies to distribute a toxicant effectively within the colony. The approach, based entirely on horizontal transfer, takes advantage of various levels of social interactions in ant colonies to disseminate a toxicant throughout the colony. Results of laboratory studies coupled with LC/MS/MS analysis demonstrate that fipronil is toxic to Argentine ants in extremely small (nanogram) quantities and is efficiently transferred from a single treated donor to multiple recipients, causing significant secondary mortality. A field study was conducted in native fynbos plots invaded by Argentine ants. The study consisted of collecting naïve workers, treating them with fipronil, and releasing them within invaded plots. Results show that the release of fipronil-treated ants reduced Argentine ant abundance by >90% within 24 h. The horizontal transfer approach offers environmental benefits with regard to pesticide use in ecologically sensitive environments and appears ideally suited for ant management in conservation areas.

Abdominal microbial communities in ants depend on colony membership rather than caste and are linked to colony productivity.

Gut bacteria aid their host in digestion and pathogen defense, and bacterial communities that differ in diversity or composition may vary in their ability to do so. Typically, the gut microbiomes of animals living in social groups converge as members share a nest environment and frequently interact. Social insect colonies, however, consist of individuals that differ in age, physiology, and behavior, traits that could affect gut communities or that expose the host to different bacteria, potentially leading to variation in the gut microbiome within colonies. Here we asked whether bacterial communities in the abdomen of Temnothorax nylanderi ants, composed largely of the gut microbiome, differ between different reproductive and behavioral castes. We compared microbiomes of queens, newly eclosed workers, brood carers, and foragers by high‐throughput 16S rRNA sequencing. Additionally, we sampled individuals from the same colonies twice, in the field and after 2 months of laboratory housing. To disentangle the effects of laboratory environment and season on microbial communities, additional colonies were collected at the same location after 2 months. There were no large differences between ant castes, although queens harbored more diverse microbial communities than workers. Instead, we found effects of colony, environment, and season on the abdominal microbiome. Interestingly, colonies with more diverse communities had produced more brood. Moreover, the queens' microbiome composition was linked to egg production. Although long‐term coevolution between social insects and gut bacteria has been repeatedly evidenced, our study is the first to find associations between abdominal microbiome characteristics and colony productivity in social insects.