Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies

In socially living animals, individuals interact through complex networks of contact that may influence the spread of disease. Whereas traditional epidemiological models typically assume no social structure, network theory suggests that an individual’s location in the network determines its risk of infection. Empirical, especially experimental, studies of disease spread on networks are lacking, however, largely due to a shortage of amenable study systems. We used automated video-tracking to quantify networks of physical contact among individuals within colonies of the social bumble bee Bombus impatiens. We explored the effects of network structure on pathogen transmission in naturally and artificially infected hives. We show for the first time that contact network structure determines the spread of a contagious pathogen (Crithidia bombi) in social insect colonies. Differences in rates of infection among colonies resulted largely from differences in network density among hives. Within colonies, a bee’s rate of contact with infected nestmates emerged as the only significant predictor of infection risk. The activity of bees, in terms of their movement rates and division of labour (e.g., brood care, nest care, foraging), did not influence risk of infection. Our results suggest that contact networks may have an important influence on the transmission of pathogens in social insects and, possibly, other social animals.     

Experimentally induced change in infectious period affects transmission dynamics in a social group

A key component of any epidemiological model is the infectious period, which greatly affects the dynamics and persistence of an infection. Social organization, leading to behavioural and spatial heterogeneities among potential susceptibles, interacts with infectious period to create different risk categories within a group. Using the honeybee (Apis mellifera) colony as a social model, a protocol that creates different infectious periods in individual bees and another that follows the diffusion of a transmittable tracer within a colony, we show experimentally how a short infectious period results in an epidemic process with low prevalence confined only to individuals at the outer edge of a group, while a long infectious period results in high prevalence distributed more universally among all the group members. We call this finding an evidence of 'organizational immunity' in a social network and propose that the honeybee colony provides a unique opportunity to test its role in social transmission processes.     

Covariation between the physiological and behavioral components of pathogen transmission: host heterogeneity determines epidemic outcomes

Although heterogeneity in contact rate, physiology, and behavioral response to infection have all been empirically demonstrated in host–pathogen systems, little is known about how interactions between individual variation in behavior and physiology scale‐up to affect pathogen transmission at a population level. The objective of this study is to evaluate how covariation between the behavioral and physiological components of transmission might affect epidemic outcomes in host populations. We tested the consequences of contact rate covarying with susceptibility, infectiousness, and infection status using an individual‐based, dynamic network model where individuals initiate and terminate contacts with conspecifics based on their behavioral predispositions and their infection status. Our results suggest that both heterogeneity in physiology and subsequent covariation of physiology with contact rate could powerfully influence epidemic dynamics. Overall, we found that 1) individual variability in susceptibility and infectiousness can reduce the expected maximum prevalence and increase epidemic variability; 2) when contact rate and susceptibility or infectiousness negatively covary, it takes substantially longer for epidemics to spread throughout the population, and rates of epidemic spread remained suppressed even for highly transmissible pathogens; and 3) reductions in contact rate resulting from infection‐induced behavioral changes can prevent the pathogen from reaching most of the population. These effects were strongest for theoretical pathogens with lower transmissibility and for populations where the observed variation in contact rate was higher, suggesting that such heterogeneity may be most important for less infectious, more chronic diseases in wildlife. Understanding when and how variability in pathogen transmission should be modelled is a crucial next step for disease ecology.     

The dynamics of sexual contact networks: effects on disease spread and control

Sexually transmitted pathogens persist in populations despite the availability of biomedical interventions and knowledge of behavioural changes that would reduce individual-level risk. While behavioural risk factors are shared between many sexually transmitted infections, the prevalence of these diseases across different risk groups varies. Understanding this heterogeneity and identifying better control strategies depends on an improved understanding of the complex social contact networks over which pathogens spread. To date, most efforts to study the impact of sexual network structure on disease dynamics have focused on static networks. However, the interaction between the dynamics of partnership formation and dissolution and the dynamics of transmission plays a role, both in restricting the effective network accessible to the pathogen, and in modulating the transmission dynamics. We present a simple method to simulate dynamical networks of sexual partnerships. We inform the model using survey data on sexual attitudes and lifestyles, and investigate how the duration of infectiousness changes the effective contact network over which disease may spread. We then simulate several control strategies: screening, vaccination and behavioural interventions. Previous theory and research has advanced the importance of core groups for spread and control of STD. Our work is consistent with the importance of core groups, but extends this idea to consider how the duration of infectiousness associated with a particular pathogen interacts with host behaviours to define these high risk subpopulations. Characteristics of the parts of the network accessible to the pathogen, which represent the network structure of sexual contacts from the “point of view” of the pathogen, are substantially different from those of the network as a whole. The pathogen itself plays an important role in determining this effective network structure; specifically, we find that if the pathogen’s duration of infectiousness is short, infection is more concentrated in high-activity, high-concurrency individuals even when all other factors are held constant. Widespread screening programmes would be enhanced by follow-up interventions targeting higher-risk individuals, because screening shortens the expected duration of infectiousness and causes a greater relative decrease in prevalence among lower-activity than in higher-activity individuals. Even for pathogens with longer durations of infectiousness, our findings suggest that targeting vaccination and behavioural interventions towards high-activity individuals provides comparable benefits to population-wide interventions.     

Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects

The role of disease in the organization of insect colonies has become an important focus of research in evolutionary pathobiology, in which the relationship of sociality and disease transmission can be comparatively and experimentally analysed. In this paper we use an individual-based model of disease transmission to assess how an epidemic is influenced by worker density and activity level, the probability of disease transmission, and the structural organization of the nest. First, we observed in our model a nonlinear interaction between worker density and the probability of disease transmission: high levels of both factors interact to enhance the likelihood of an epidemic. Additionally, when we incorporated in our model the empirical observation that only a fraction of the worker population in social insect colonies is active at any given point in time, results suggested that relatively low levels of worker movement can have a significant impact on the spread of disease, slowing its transmission through the colony. Finally, we found that nests having even a simple spatial separation of chambers could delay the spread of infection and diminish the severity of an outbreak. The effect of nest structure in delaying infection spread became more pronounced as nest architecture became increasingly unidimensional, as in the case of simple gallery nests. Therefore, nest architecture and worker activity patterns might indeed exert considerable influence on the dynamics of epidemics in social insects and should be incorporated into models of disease transmission.     

The influence of social hunger on food distribution and its implications for disease transmission in a honeybee colony

Social insect colonies are characterized by extensive interactions among individuals, exchanges that can also potentially transmit pathogens. The large majority of these social interactions in a honeybee colony result from food transfer among individuals. Since colony hunger is likely to have a significant influence on these interactions, we investigated its effect on the distribution of food within the colony. By pulsing two colonies having different amounts of stored food with a radioactive label, we found that a starved colony sent out a larger number of foragers, brought in more food, and stored more of it than the satiated colony. We also found that the food brought into a starved colony was distributed more uniformly within each age class than that in the satiated colony. The queen and the young individuals received the lowest exposure to the label even though the label entered different regions of the colony at the same rate. The satiation level of the colony did not influence the relative exposures of different age groups to the label but a higher amount of it was stored in the hungry colony. We discuss the significance of these results in terms of the role played by the organizational structure of the honeybee colony on the transmission dynamics of an infectious disease.     

Colony-size effects on task organization in the harvester ant Pogonomyrmex californicus

Colony size is a fundamental attribute of insect societies that appears to play an important role in their organization of work. In the harvester ant Pogonomyrmex californicus, division of labor increases with colony size during colony ontogeny and among unmanipulated colonies of the same age. However, the mechanism(s) integrating individual task specialization and colony size is unknown. To test whether the scaling of division of labor is an emergent epiphenomenon, as predicted by self-organizational models of task performance, we manipulated colony size in P. californicus and quantified short-term behavioral responses of individuals and colonies. Variation in colony size failed to elicit a change in division of labor, suggesting that colony-size effects on task specialization are mediated by slower developmental processes and/or correlates of colony size that were missing from our experiment. In contrast, the proportional allocation of workers to tasks shifted with colony size, suggesting that task needs or priorities depend, in part, on colony size alone. Finally, although task allocation was flexible, colony members differed consistently in task performance and spatial tendency across colony size treatments. Sources of interindividual behavioral variability include worker age and genotype (matriline).     

Revealing mechanisms of infectious disease spread through empirical contact networks

The spread of pathogens fundamentally depends on the underlying contacts between individuals. Modeling the dynamics of infectious disease spread through contact networks, however, can be challenging due to limited knowledge of how an infectious disease spreads and its transmission rate. We developed a novel statistical tool, INoDS (Identifying contact Networks of infectious Disease Spread) that estimates the transmission rate of an infectious disease outbreak, establishes epidemiological relevance of a contact network in explaining the observed pattern of infectious disease spread and enables model comparison between different contact network hypotheses. We show that our tool is robust to incomplete data and can be easily applied to datasets where infection timings of individuals are unknown. We tested the reliability of INoDS using simulation experiments of disease spread on a synthetic contact network and find that it is robust to incomplete data and is reliable under different settings of network dynamics and disease contagiousness compared with previous approaches. We demonstrate the applicability of our method in two host-pathogen systems: Crithidia bombi in bumblebee colonies and Salmonella in wild Australian sleepy lizard populations. INoDS thus provides a novel and reliable statistical tool for identifying transmission pathways of infectious disease spread. In addition, application of INoDS extends to understanding the spread of novel or emerging infectious disease, an alternative approach to laboratory transmission experiments, and overcoming common data-collection constraints.     

Raccoon Social Networks and the Potential for Disease Transmission

Raccoons are an important vector of rabies and other pathogens. The degree to which these pathogens can spread through a raccoon population should be closely linked to association rates between individual raccoons. Most studies of raccoon sociality have found patterns consistent with low levels of social connectivity within populations, thus the likelihood of direct pathogen transmission between raccoons is theoretically low. We used proximity detecting collars and social network metrics to calculate the degree of social connectivity in an urban raccoon population for purposes of estimating potential pathogen spread. In contrast to previous assumptions, raccoon social association networks were highly connected, and all individuals were connected to one large social network during 15 out of 18 months of study. However, these metrics may overestimate the potential for a pathogen to spread through a population, as many of the social connections were based on relatively short contact periods. To more closely reflect varying probabilities of pathogen spread, we censored the raccoon social networks based on the total amount of time spent in close proximity between two individuals per month. As this time criteria for censoring the social networks increased from one to thirty minutes, corresponding measures of network connectivity declined. These findings demonstrate that raccoon populations are much more tightly connected than would have been predicted based on previous studies, but also point out that additional research is needed to calculate more precise transmission probabilities by infected individuals, and determine how disease infection changes normal social behaviors.     

TB-infected deer are more closely related than non-infected deer

Identifying mechanisms of pathogen transmission is critical to controlling disease. Social organization should influence contacts among individuals and thus the distribution and spread of disease within a population. Molecular genetic markers can be used to elucidate mechanisms of disease transmission in wildlife populations without undertaking detailed observational studies to determine probable contact rates. Estimates of genealogical relationships within a bovine tuberculosis-infected white-tailed deer (Odocoileus virginianus) population indicated that infected deer were significantly more closely related than non-infected deer suggesting that contact within family groups was a significant mechanism of disease transmission. Results demonstrate that epidemiological models should incorporate aspects of host ecology likely to affect the probability of disease transmission.     

Percent lipid is associated with body size but not task in the bumble bee <Emphasis Type="Italic">Bombus impatiens</Emphasis>

In some group-living organisms, labor is divided among individuals. This allocation to particular tasks is frequently stable and predicted by individual physiology. Social insects are excellent model organisms in which to investigate the interplay between physiology and individual behavior, as division of labor is an important feature within colonies, and individual physiology varies among the highly related individuals of the colony. Previous studies have investigated what factors are important in determining how likely an individual is, compared to nestmates, to perform certain tasks. One such task is foraging. Corpulence (i.e., percent lipid) has been shown to determine foraging propensity in honey bees and ants, with leaner individuals being more likely to be foragers. Is this a general trend across all social insects? Here we report data analyzing the individual physiology, specifically the percent lipid, of worker bumble bees (Bombus impatiens) from whom we also analyze behavioral task data. Bumble bees are also unusual among the social bees in that workers may vary widely in size. Surprisingly we find that, unlike other social insects, percent lipid is not associated with task propensity. Rather, body size closely predicts individual relative lipid stores, with smaller worker bees being allometrically fatter than larger worker bees.     

Using social networks to deduce whether residents or dispersers spread parasites in a lizard population

1. Heterogeneity of host behaviour can play an important role in the spread of parasites and pathogens around wildlife populations. Social networks have previously been suggested to represent transmission pathways within a population, but where the dynamics of host-parasite interactions are difficult to observe, networks may also be used to provide insights into transmission processes. 2. Pygmy bluetongue lizards, Tiliqua adelaidensis, occupy individual territories, live exclusively in burrows constructed by spiders in Australian native grasslands and are hosts to a tick, Bothriocroton hydrosauri, and a nematode, Pharyngodon wandillahensis. 3. On five monthly occasions, the locations of all individual lizards in three study plots were used to construct weighted, undirected networks based on proximity of adjacent burrows. 4. The networks were used to explore alternative hypotheses about the spread of each parasite through the population: that stable population members that remained in the same burrow over the study period played a major role in influencing the pattern of infection or that dispersing individuals played a more significant role. 5. For ticks, host individuals that were infected were more connected in the network than uninfected hosts and this relationship remained significant for connections to residents in the population, but not for connections to dispersers. 6. For nematodes, infected and uninfected hosts did not differ in their overall strength of connection in the network, but infected hosts were more connected to dispersers than were uninfected hosts, suggesting that lizards moving across the population are the major agents for the transmission of nematodes. 7. This study shows how network analyses can provide new insights into alternative pathways of parasite spread in wildlife populations, where it is difficult to make direct observations of transmission-related behaviours.     

Spread of plague among black-tailed prairie dogs is associated with colony spatial characteristics

Sylvatic plague (Yersinia pestis) is an exotic pathogen that is highly virulent in black-tailed prairie dogs (Cynomys ludovicianus) and causes widespread colony losses and individual mortality rates >95%. We investigated colony spatial characteristics that may influence inter-colony transmission of plague at 3 prairie dog colony complexes in the Great Plains. The 4 spatial characteristics we considered include: colony size, Euclidean distance to nearest neighboring colony, colony proximity index, and distance to nearest drainage (dispersal) corridor. We used multi-state mark–recapture models to determine the relationship between these colony characteristics and probability of plague transmission among prairie dog colonies. Annual mapping of colonies and mark–recapture analyses of disease dynamics in natural colonies led to 4 main results: 1) plague outbreaks exhibited high spatial and temporal variation, 2) the site of initiation of epizootic plague may have substantially influenced the subsequent inter-colony spread of plague, 3) the long-term effect of plague on individual colonies differed among sites because of how individuals and colonies were distributed, and 4) colony spatial characteristics were related to the probability of infection at all sites although the relative importance and direction of relationships varied among sites. Our findings suggest that conventional prairie dog conservation management strategies, including promoting large, highly connected colonies, may need to be altered in the presence of plague. © 2011 The Wildlife Society     

Individual experience alone can generate lasting division of labor in ants

Division of labor, the specialization of workers on different tasks, largely contributes to the ecological success of social insects [1, 2]. Morphological, genotypic, and age variations among workers, as well as their social interactions, all shape division of labor [1-12]. In addition, individual experience has been suggested to influence workers in their decision to execute a task [13-18], but its potential impact on the organization of insect societies has yet to be demonstrated [19, 20]. Here we show that, all else being equal, ant workers engaged in distinct functions in accordance with their previous experience. When individuals were experimentally led to discover prey at each of their foraging attempts, they showed a high propensity for food exploration. Conversely, foraging activity progressively decreased for individuals who always failed in the same situation. One month later, workers that previously found prey kept on exploring for food, whereas those who always failed specialized in brood care. It thus appears that individual experience can strongly channel the behavioral ontogeny of ants to generate a lasting division of labor. This self-organized task-attribution system, based on an individual learning process, is particularly robust and might play an important role in colony efficiency.     

Seasonal variation in daily patterns of social contacts in the European badger Meles meles

Social interactions among hosts influence the persistence and spread of infectious pathogens. Daily and seasonal variation in the frequency and type of social interactions will play an important role in disease epidemiology and, alongside other factors, may have an influence on wider disease dynamics by causing seasonal forcing of infection, especially if the seasonal variation experienced by a population is considerable. We explored temporal variation in within‐group contacts in a high‐density population of European badgers Meles meles naturally infected with Mycobacterium bovis (the causative agent of bovine tuberculosis). Summer contacts were more likely and of longer duration during the daytime, while the frequency and duration of winter contacts did not differ between day and night. In spring and autumn, within‐group contacts peaked at dawn and dusk, corresponding with when they were of shortest duration with reduced potential for aerosol transmission of pathogens. Summer and winter could be critical for transmission of M. bovis in badgers, due to the high frequency and duration of contacts during resting periods, and we discuss the links between this result and empirical disease data. This study reveals clear seasonality in daily patterns of contact frequency and duration in species living in stable social groups, suggesting that changes in social contacts could drive seasonal forcing of infection in wildlife populations even when the number of individuals interacting remains similar.     

Response thresholds alone cannot explain empirical patterns of division of labor in social insects

The effects of heterogeneity in group composition remain a major hurdle to our understanding of collective behavior across disciplines. In social insects, division of labor (DOL) is an emergent, colony-level trait thought to depend on colony composition. Theoretically, behavioral response threshold models have most commonly been employed to investigate the impact of heterogeneity on DOL. However, empirical studies that systematically test their predictions are lacking because they require control over colony composition and the ability to monitor individual behavior in groups, both of which are challenging. Here, we employ automated behavioral tracking in 120 colonies of the clonal raider ant with unparalleled control over genetic, morphological, and demographic composition. We find that each of these sources of variation in colony composition generates a distinct pattern of behavioral organization, ranging from the amplification to the dampening of inherent behavioral differences in heterogeneous colonies. Furthermore, larvae modulate interactions between adults, exacerbating the apparent complexity. Models based on threshold variation alone only partially recapitulate these empirical patterns. However, by incorporating the potential for variability in task efficiency among adults and task demand among larvae, we account for all the observed phenomena. Our findings highlight the significance of previously overlooked parameters pertaining to both larvae and workers, allow the formulation of theoretical predictions for increasing colony complexity, and suggest new avenues of empirical study.

This study uses automated tracking of clonal raider ants and mathematical modeling to reveal how previously overlooked traits of larvae and workers might shape social organization in heterogeneous ant colonies. By incorporating the potential for variability in task efficiency among adults and task demand among larvae, the authors were able to account for all empirically observed phenomena.     

Equal graph partitioning on estimated infection network as an effective epidemic mitigation measure

Controlling severe outbreaks remains the most important problem in infectious disease area. With time, this problem will only become more severe as population density in urban centers grows. Social interactions play a very important role in determining how infectious diseases spread, and organization of people along social lines gives rise to non-spatial networks in which the infections spread. Infection networks are different for diseases with different transmission modes, but are likely to be identical or highly similar for diseases that spread the same way. Hence, infection networks estimated from common infections can be useful to contain epidemics of a more severe disease with the same transmission mode. Here we present a proof-of-concept study demonstrating the effectiveness of epidemic mitigation based on such estimated infection networks. We first generate artificial social networks of different sizes and average degrees, but with roughly the same clustering characteristic. We then start SIR epidemics on these networks, censor the simulated incidences, and use them to reconstruct the infection network. We then efficiently fragment the estimated network by removing the smallest number of nodes identified by a graph partitioning algorithm. Finally, we demonstrate the effectiveness of this targeted strategy, by comparing it against traditional untargeted strategies, in slowing down and reducing the size of advancing epidemics.     

Foraging responses ofFormica truncorum (Hymenoptera; Formicidae); exploiting stable vs spatially and temporally variable resources

Summary Social organization allows a division of labor between reproduction and foraging, as well as a task allocation among foraging individuals. Therefore, a colony simultaneously exploiting various resources can use different ways of getting them. This work analyzes wood ant foraging tactics both at the collective and the individual level. The main issues are: (1) How does a wood ant colony respond to stable vs temporally and spatially variable resources in terms of worker force allocation? (2) How is retrieval of ephemeral but rich resources effected at the individual level? The results show a correspondence between resource stability and behavior. Ants visited stable resources continually and recruited to ephemeral ones. They also visited empty food sites at a low frequency suggesting territoriality and constant scanning. The results suggest that recruitment may involve defence of the resource, since only a small fraction of all the workers available carry the food home. Additional ants arriving at the resource are recruited from inside the nest, not by reallocating outdoor workers. The foragers also form two separate groups, one site-persistent and another site-flexible. These two forager groups may reflect specialization on two different kinds of diet: honeydew or insect prey (spatially and temporally stable vs unstable resources, respectively).Formica truncorum is thus an example of how sociality allows the use of two different foraging strategies simultaneously: one that is based on recruitment to ephemeral resources and another that is based on search persistance and memory.     

Social inhibition and the regulation of temporal polyethism in honey bees.

Honey bee division of labor is characterized by temporal polyethism, in which young workers remain in the hive and perform tasks there, whereas old workers perform more risky outside tasks, mainly foraging. We present a model of honey bee division of labor based on (1) an intrinsic process of behavioral development and (2) inhibition of development through social interactions among the workers in a colony. The model shows that these two processes can explain the main features of honey bee temporal polyethism: the correlation between age and task performance; the age at which a worker first forages and how this age varies among hives; the balanced allocation of workers to hive tasks and foraging; the recovery of a colony from demographic perturbations; and the differentiation of workers into different behavioral roles. The model provides a baseline picture of individual and colony behavior that can serve as the basis for studies of more fine-grained regulation of division of labor.