Social Immunity

Concept

Social immunity is a recently developed concept used to describe the evolution of an additional level of immunity in the colonies of eusocial insects (some bees and wasps, all ants and termites). It is equally used to describe collective disease defences in other stable societies, including those of primates, and, has also been broadened to include other social interactions, such as parental care.

Social immunity provides an integrated approach for the study of disease dynamics in societies, combining both the behaviour and physiology (including molecular-level processes) of all group members and their social interactions. It thereby links the fields of social evolution and ecological immunology. Social immunity also affects epidemiology, as it can impact both the course of an infection at the individual level, as well as the spread of disease within the group.

Social immunity differs from similar phenomena that can occur in groups that are not truly social (e.g. herding animals). These include (i) density dependent prophylaxis, which is the up regulation of the individual immunity of group members under temporal crowding, and (ii) herd immunity, which is the protection of susceptible individuals in an otherwise immune group, where pathogens are unable to spread due to the high ratio of immune to suceptible hosts. Further, although social immunity can be achieved through behavioural, physiological or organisational defences, these components are not mutually exclusive and often overlap. For example, organisational defences, such as an altered interaction network that influences disease spread, emerge from chemical and behavioural processes.

Disease risk in social groups

Sociality, although a very successful way of life, is thought to increase the per-individual risk of acquiring disease, simply because close contact with conspecifics is a key transmission route for infectious diseases. As social organisms are often densely aggregated and exhibit high levels of interaction, pathogens can more easily spread from infectious to susceptible individuals. The intimate interactions often found in social insects, such as the sharing of food through regurgitation, are further possible routes of pathogen transmission. As the members of social groups are typically closely related, they are more likely to be susceptible to the same pathogens. This effect is compounded when overlapping generations are present (such as in social insect colonies and primate groups), which facilitates the horizontal transmission of pathogens from the older generation to the next. In the case of species that live in nests/burrows, stable, homeostatic temperatures and humidity may create ideal conditions for pathogen growth.

Disease risk is further affected by the ecology. For example, many social insects nest and forage in habitats that are rich in pathogens, such as soil or rotting wood, exposing them to a plethora of microparasites, e.g. fungi, bacteria, viruses and macroparasites, e.g. mites and nematodes. In addition, shared food resources, such as flowers, can act as disease hubs for social insect pollinators, promoting both interspecific and intraspecific pathogen transmission. This may be a contributing factor in the spread of emergent infectious diseases in bees.

All of these factors combined can therefore contribute to rapid disease spread following an outbreak, and, if transmission is not controlled, an epizootic (an animal epidemic) may result. Hence, social immunity has evolved to reduce and mitigate this risk.

Nest hygiene

Social insects have evolved an array of sanitary behaviours to keep their nests clean, thereby reducing the probability of parasite establishment and spread within the colony. Such behaviours can be employed either prophylactically, or actively, upon demand. For example, social insects can incorporate materials with antimicrobial properties into their nest, such as conifer resin, or faecal pellets that contain symbiont derived antimicrobials. These materials reduce the growth and density of many detrimental bacteria and fungi. Antimicrobial substances can also be self-produced. Secretions from the metapleural glands of ants and volatile chemical components produced by termites have been shown to inhibit fungal germination and growth. Another important component of nest hygiene is waste management, which involves strict spatial separation of clean nest areas and waste dumps. Social insect colonies often deposit their waste outside of the nest, or in special compartments, including waste chambers for food leftovers, “toilets” for defecation and “graveyards”, where dead individuals are deposited, reducing the probability of parasite transmission from potentially infected cadavers. Where social insects place their waste is also important. For example, leaf cutting ants living in xeric conditions deposit their waste outside the nest, whilst species living in the tropics tend to keep it in special chambers within the nest. It has been proposed that this difference is related to the likelihood that the external environment reduces or enhances microbial growth. For xeric-living ants, placing waste outside will tend to inhibit infectious material, as microbes are usually killed under hot, dry conditions. On the other hand, placing waste into warm, humid environments will promote microbial growth and disease transmission, so it may be safer for ants living in the topics to contain their waste within the nest. Honeybees have evolved the ability to actively maintain a constant temperature within their hives to ensure optimal brood development. Upon exposure to Ascoshpaera apis, a heat sensitive fungal pathogen that causes chalk brood, honeybees increase the temperature of the brood combs, thereby creating conditions that disfavour the growth of the pathogen. This "social fever" is performed before symptoms of the disease are expressed and can therefore be viewed as a preventative measure to avoid chalk brood outbreaks in the colony.

Sanitary care of group members

Sanitary care reduces the risk of infection for group members and can slow the course of disease. For example, grooming is the first line of defence against externally-infected pathogens such as entomopathogenic fungi, whose infectious conidia can be mechanically removed through self- and allogrooming (social grooming) to prevent infection. As conidia of such fungi only loosely attach to the cuticle of the host to begin with, grooming can dramatically reduce the number of infective stages. Although grooming is also performed often in the absence of a pathogen, it is an adaptive response, with both the frequency and duration of grooming (self and allo) increasing when pathogen exposure occurs. In several species of social insect, allogrooming of contaminated workers has been shown to dramatically improve survival, compared to single workers that can only conduct self-grooming.

In the case of ants, pathogens large enough to be removed by grooming are first collected into the infrabuccal pocket (found in the mouth), which prevents the pathogens entering the digestive system. In the pocket, they may be mixed labial gland secretions or with poison the ants have taken up into their mouths. These compounds reduce germination viability, rendering conidia non-infectious when later expelled as an infrabuccal pellet. In the case of termites, pathogens removed during grooming are not filtered out before entering the gut, but are allowed to pass through the digestive tract. Symbiotic microorganisms in the hindgut of the termite are also able to deactivate pathogens, rendering them non-infectious when they are excreted.

In addition to grooming, social insects can apply host- and symbiont-derived antimicrobial compounds to themselves and each other to inhibit pathogen growth or germination. In ants, the application of antimicrobials is often performed in conjunction with grooming, to provide simultaneous mechanical removal and chemical treatment of pathogens. In ants, poison can be taken up into the mouth from the acidopore (the exit of the poison producing gland at the tip of the abdomen), and stored in the mouth, to be redistributed whilst grooming. In the ant Lasius neglectus, the poison produced by the acidopore is composed largely of formic acid (60%), but also contains acetic acid (2%). Inhibition assays of the poison droplet against the fungal pathogen Metarhizium found that the formic acid alone substantially reduces fungal conidia viability, but that all poison components work synergistically to inhibit conidia viability, by as much as 96%.

Dealing with infected group members

Infected individuals and diseased corpses pose a particular risk for social insects because they can act a source of infection for the rest of the colony. As mentioned above, dead nestmates are typically removed from the nest to reduce the potential risk of disease transmission. Infected or not, ants that are close to death can also voluntarily remove themselves from the colony to limit this risk. Honeybees can actively drag infected nest mates out of the hive and may bar them from entering at all. "Hygienic behaviour" is the specific removal of infected brood from the colony and has been reported in both honeybees and ants. In honeybees, colonies have been artificially selected to perform this behavior faster. These "hygienic" hives have improved recovery rates following brood infections, as the earlier infected brood is removed, the less likely it is to have become contagious already. Cannibalism of infected nesmtates is an effective behaviour in termites, as ingested infectious material is destroyed by antimicrobial enzymes present in their guts. These enzymes function by breaking down the cell walls of pathogenic fungi, for example, and are produced both by the termite itself and their gut microbiota. If there are too many corpses to cannibalise, termites bury them in the nest instead. Like removal in ants and bees, this isolates the corpses to contain the pathogen, but does not prevent their replication. Some fungal pathogens (e.g. Ophiocordyceps, Pandora) manipulate their ant hosts into leaving the nest and climbing plant stems surrounding the colony. There, attached to the stem, they die and rain down new spores onto healthy foragers. To combat these fungi, healthy ants actively search for corpses on plant stems and attempt to remove them before they can release their spores

Colony-level immunisation

Immunisation is a reduced susceptibility to a parasite upon secondary exposure to the same parasite. The past decade has revealed that immunisation occurs in invertebrates and is active against a wide rage of parasites. It occurs in two forms: (i) specific immune priming particular parasite or (ii) a general immune up-regulation that promotes unspecific protection against a broad range of parasites. In any case, the underlying mechanisms of immunisation in invertebrates are still mostly elusive. In social animals, immunisation is not restricted to the level of the individual, but can also occur at the society level, via 'social immunisation'. Social immunisation occurs when some proportion of the group's members are exposed to a parasite, which then leads to the protection of the whole group, upon secondary contact to the same parasite. Social immunisation has been so far described in a dampwood termite-fungus system, a garden ant-fungus system and a carpenter ant–bacterium system. In all cases, social contact with pathogen-exposed individuals promoted reduced susceptibility in their nestmates (increased survival), upon subsequent exposure to the same pathogen. In the ant-fungus and termite-fungus systems, social immunisation was shown to be caused by the transfer of fungal conidia during allogrooming, from the exposed insects to nestmates performing grooming. This contamination resulted in low-level infections of the fungus in the nestmates, which stimulated their immune system, and protected them against subsequent lethal exposures to the same pathogen. This method of immunisation parallels variolation, an early form of human vaccination, which used live pathogens to protect patients against, for example, smallpox

Organisational defence

Organisational disease defence — or organisational immunity — refers to patterns of social interactions which could, hypothetically, mitigate disease transmission in a social group. As disease transmission occurs through social interactions, changes in the type and frequency of these interactions are expected to modulate disease spread. Organisational immunity is predicted to have both a constitutive and an induced component. The innate, organisational substructure of social insect colonies may provide constitutional protection of the most valuable colony members, the queens and brood, as disease will be contained within subgroups. Social insect colonies are segregated into worker groups that experience different disease hazards, where the young and reproductive individuals interact minimally with the workers performing the tasks with higher disease risk (e.g. foragers). This segregation can arise as a result of the physical properties of the nest or the differences in space usage of the individuals. It can also result from age- or task-biased interactions. Distinct activity patterns between group members (e.g. individuals with relatively higher number of interactions, or high number of interaction partners) has also been hypothesized to influence disease spread. It is further assumed that social insects may further modulate their interaction networks upon disease coming into the colony. However, the organisational immunity hypothesis is currently mainly supported by theoretical models and awaits empirical testing.