Mechanisms Of Social Immunity Research Articles

The Mechanisms of Social Immunity Against Fungal Infections in Eusocial Insects.

Entomopathogenic fungus as well as their toxins is a natural threat surrounding social insect colonies. To defend against them, social insects have evolved a series of unique disease defenses at the colony level, which consists of behavioral and physiological adaptations. These colony-level defenses can reduce the infection and poisoning risk and improve the survival of societal members, and is known as social immunity. In this review, we discuss how social immunity enables the insect colony to avoid, resist and tolerate fungal pathogens. To understand the molecular basis of social immunity, we highlight several genetic elements and biochemical factors that drive the colony-level defense, which needs further verification. We discuss the chemosensory genes in regulating social behaviors, the antifungal secretions such as some insect venoms in external defense and the immune priming in internal defense. To conclude, we show the possible driving force of the fungal toxins for the evolution of social immunity. Throughout the review, we propose several questions involved in social immunity extended from some phenomena that have been reported. We hope our review about social ‘host–fungal pathogen’ interactions will help us further understand the mechanism of social immunity in eusocial insects.

Israeli Acute Paralysis Virus: Honey Bee Queen⁻Worker Interaction and Potential Virus Transmission Pathways.

Queen loss or failure is an important cause of honey bee colony loss. A functional queen is essential to a colony, and the queen is predicted to be well protected by worker bees and other mechanisms of social immunity. Nevertheless, several honey bee pathogens (including viruses) can infect queens. Here, we report a series of experiments to test how virus infection influences queen–worker interactions and the consequences for virus transmission. We used Israeli acute paralysis virus (IAPV) as an experimental pathogen because it is relevant to bee health but is not omnipresent. Queens were observed spending 50% of their time with healthy workers, 32% with infected workers, and 18% without interaction. However, the overall bias toward healthy workers was not statistically significant, and there was considerable individual to individual variability. We found that physical contact between infected workers and queens leads to high queen infection in some cases, suggesting that IAPV infections also spread through close bodily contact. Across experiments, queens exhibited lower IAPV titers than surrounding workers. Thus, our results indicate that honey bee queens are better protected by individual and social immunity, but this protection is insufficient to prevent IAPV infections completely.

Brood Affects Hygienic Behavior in the Honey Bee (Hymenoptera: Apidae).

Despite receiving much attention, the ectoparasitic mite Varroa destructor (Anderson and Trueman) and the pathogens it vectors remain critical threats to the health of the honey bee Apis mellifera (Linnaeus) (Hymenoptera: Apidae). One promising intervention approach is the breeding of hygienic honey bees, which have an improved ability to detect and remove unhealthy brood from the colony, and are thus more resistant to Varroa. While much hygienic behavior-related research has focused on enhanced adult honey bee olfaction, less attention has been paid to the olfactory signals that originate inside the brood cell, triggering hygienic removal. Here, we hypothesized that selection for hygienic behavior in honey bees has influenced brood signaling, predicting that: 1) in a common social environment, removal rates differ among brood with different selective breeding histories, and 2) the removal rates of brood positively correlate to the hygiene level of the brood's colony of origin. To test these predictions, we cross-fostered brood subjected to control, wound, or Varroa treatment in unselected (UNS), Minnesota Hygienic (HYG), and Varroa-Sensitive Hygienic (VSH) colonies, and monitored individual brood cells for hygienic removal. Results confirmed both predictions, as brood from hygienic colonies was more likely to be removed than brood from UNS colonies, regardless of where the brood was fostered. These findings suggest that hygiene-related brood signals complement previously identified characteristics of hygienic adults, constituting an important mechanism of social immunity in honey bees. Thus, selective breeding for honey bee hygienic behavior may be improved through the utilization of field assays containing compounds related to larval signaling.

Inducible versus constitutive social immunity: examining effects of colony infection on glucose oxidase and defensin-1 production in honeybees.

Honeybees use a variety of defence mechanisms to reduce disease infection and spread throughout the colony. Many of these defences rely on the collective action of multiple individuals to prevent, reduce or eradicate pathogens—often referred to as ‘social immunity’. Glucose oxidase (GOX) and some antimicrobial peptides (e.g. defensin-1 or Def1) are secreted by the hypopharyngeal gland of adult bees on larval food for their antiseptic properties. Because workers secrete these compounds to protect larvae, they have been used as ‘biomarkers’ for social immunity. The aim of this study was to investigate if GOX and Def1 are induced after pathogen exposure to determine whether its production by workers is the result of a collective effort to protect the brood and colony in response to a pathogen challenge. Specifically, we quantified GOX and Def1 in honeybee adults before and after colony-level bacterial infection by American foulbrood ((AFB), Paenibacillus larvae). Overall, our results indicate that levels of GOX and Def1 are not induced in response to pathogenic infections. We therefore conclude that GOX and Def1 are highly constitutive and co-opted as mechanisms of social immunity, and these factors should be considered when investigating immunity at the individual and colony level in social insects.

Cuticular hydrocarbon cues of immune-challenged workers elicit immune activation in honeybee queens.

Recently, evidence has shown that variations in the cuticular hydrocarbons (CHCs) profile allow healthy honeybees to identify diseased nestmates, eliciting agonistic responses in the former. Here, we determined whether these 'immunologic cues' emitted by diseased nestmates were only detected by workers, who consequently took hygienic measures and excluded these individuals from the colony, or whether queens were also able to detect these cues and respond accordingly. Healthy honeybee queens were exposed to (i) healthy, (ii) Ringer-injected and (iii) lipopolysaccharide (LPS)-injected nestmates by allowing direct body contact. Quantitative differences in the CHC profiles of these three groups were measured using GC-MS. The transcript levels of the products of four genes that encode for antimicrobial peptides (AMPs), which are part of the queen's immune response, were measured in bees exposed to direct contact using qPCR. A significant increase in the transcript levels of these AMP genes over baseline levels in queens was observed when body contact was allowed between the queens and the Ringer- and LPS-injected nestmates. These results provide the first evidence that the detection of CHCs contributes to the initiation of an immune response in insects. In an additional experiment, CHCs were extracted from diseased workers and directly presented to queens, which also evoked a similar immune response. A potential mechanism that relied on volatile compounds could be ruled out by conducting a distance experiment. The study helps to expand our knowledge of chemical communication in insects and sheds light on a likely new mechanism of social immunity.

Automated assay and differential model of western honey bee (Apis mellifera) autogrooming using digital image processing

In animals, self-grooming is an important component of their overall hygiene because it reduces the risk of disease and parasites. The European honey bee (Apis mellifera) exhibits hygienic behavior, which refers to the ability of the members of a colony to remove diseased or dead brood from the hive. Individual grooming behavior, however, is when a bee grooms itself to remove parasites. While both behaviors are critical for the mitigation of disease, hygienic behavior is overwhelmingly more studied because, unlike grooming behavior, it has a simple bioassay to measure its phenotype. Here, we develop a novel bioassay to expedite data collection of grooming behavior by testing different honey bee genotypes (stocks). Individual worker bees from different commercial stocks were coated in baking flour, placed in an observation arena, and digitally recorded to automatically measure grooming rates. The videos were analyzed in MATLAB, and an exponential function was fit to the pixel data to calculate individual grooming rates. While bees from the different commercial stocks were not significantly different in their grooming rates, the automation of grooming measurements may facilitate future research and stock selection for this important mechanism of social immunity.

Disease in the Society: Infectious Cadavers Result in Collapse of Ant Sub-Colonies.

Despite the growing number of experimental studies on mechanisms of social immunity in ant societies, little is known about how social behavior relates to disease progression within the nests of ants. In fact, when empirically studying disease in ant societies, it is common to remove dead ants from experiments to confirm infection by the studied parasite. This unfortunately does not allow disease to progress within the nest as it may be assumed would happen under natural conditions. Therefore, the approach taken so far has resulted in a limited knowledge of diseases dynamics within the nest environment. Here we introduced a single infectious cadaver killed by the fungus Beauveria bassiana into small nests of the ant Camponotus castaneus. We then observed the natural progression of the disease by not removing the corpses of the ants that died following the first entry of the disease. Because some behaviors such as social isolation of sick individuals or the removal of cadavers by nestmates are considered social immune functions and thus adaptations at the colony level that reduce disease spread, we also experimentally confined some sub-colonies to one or two chamber nests to prevent the expression of such behaviors. Based on 51 small nests and survival studies in 1,003 ants we found that a single introduced infectious cadaver was able to transmit within the nest, and social immunity did not prevent the collapse of the small sub-colonies here tested. This was true whether ants did or did not have the option to remove the infectious cadaver. Therefore, we found no evidence that the typically studied social immunity behaviors can reduce disease spread in the conditions here tested.

Genetic diversity confers colony-level benefits due to individual immunity.

Several costs and benefits arise as a consequence of eusociality and group-living. With increasing group size, spread of disease among nest-mates poses selective pressure on both individual immunity and group-level mechanisms of disease resistance (social immunity). Another factor known to influence colony-level expression of disease is intracolony genetic diversity, which in honeybees (Apis mellifera) is a direct function of the number of mates of the queen. Colonies headed by queens with higher mating numbers have less variable infections of decreased intensity, though the underlying mechanisms remain unclear. By pathogen-challenging larvae in vitro, we decoupled larval immune response from mechanisms of social immunity. Our results show that baseline immunity and degree of immune response do not vary with genetic diversity. However, intracolony variance in antimicrobial peptide production after pathogen challenge decreases with increasing genetic diversity. This reduction in variability of the larval immune response could drive the mitigation of disease observed in genetically diverse colonies.

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.

The Immuno-Dynamics of Conflict Intervention in Social Systems

We present statistical evidence and dynamical models for the management of conflict and a division of labor (task specialization) in a primate society. Two broad intervention strategy classes are observed– a dyadic strategy – pacifying interventions, and a triadic strategy –policing interventions. These strategies, their respective degrees of specialization, and their consequences for conflict dynamics can be captured through empirically-grounded mathematical models inspired by immuno-dynamics. The spread of aggression, analogous to the proliferation of pathogens, is an epidemiological problem. We show analytically and computationally that policing is an efficient strategy as it requires only a small proportion of a population to police to reduce conflict contagion. Policing, but not pacifying, is capable of effectively eliminating conflict. These results suggest that despite implementation differences there might be universal features of conflict management mechanisms for reducing contagion-like dynamics that apply across biological and social levels. Our analyses further suggest that it can be profitable to conceive of conflict management strategies at the behavioral level as mechanisms of social immunity.

Altruistic self‐removal of health‐compromised honey bee workers from their hive

Social insect colonies represent distinct units of selection. Most individuals evolve by kin selection and forgo individual reproduction. Instead, they display altruistic food sharing, nest maintenance and self-sacrificial colony defence. Recently, altruistic self-removal of diseased worker ants from their colony was described as another important kin-selected behaviour. Here, we report corroborating experimental evidence from honey bee foragers and theoretical analyses. We challenged honey bee foragers with prolonged CO(2) narcosis or by feeding with the cytostatic drug hydroxyurea. Both treatments resulted in increased mortality but also caused the surviving foragers to abandon their social function and remove themselves from their colony, resulting in altruistic suicide. A simple model suggests that altruistic self-removal by sick social insect workers to prevent disease transmission is expected under most biologically plausible conditions. The combined theoretical and empirical support for altruistic self-removal suggests that it may be another important kin-selected behaviour and a potentially widespread mechanism of social immunity.