Social immunity

Source: Wikipedia, the free encyclopedia.
For other uses, see Herd immunity.
A giant moray eel being cleaned
a burying beetle
Allogrooming monkeys
Human surgery
Social immunity adaptations are found in numerous branches of the tree of life, from microbes to humans

Social immunity is any antiparasite defence mounted for the benefit of individuals other than the actor. For

polyandry
.

Social immunity (also termed collective immunity) describes the additional level of disease protection arising in social groups from collective

prophylactically
or on demand.

Definition

Grooming is a key social immune defence. Here, Lasius neglectus ants groom a pathogen-exposed (red colour mark) ant to remove infectious stages of the fungus Metarhizium from its body surface, thereby reducing its risk of infection.

Sylvia Cremer defined social immunity in her seminal 2007 Current Biology paper 'Social Immunity' as the "collective action or

eusocial insects.[1][2] Cremer's definition focused on the collective benefits of behaviours and was adopted by other behavioural ecologists (e.g. Wilson-Rich 2009[3]) when describing immune phenomena which were contingent on the action of multiple individuals.[1][2] Cremer went on to develop a series of comparisons between personal and social immune systems—she explained that her definition of social immunity encompassed "the nature of these defences that they cannot be performed efficiently by single individuals, but depend strictly on the cooperation of at least two individuals".[4] However, in 2010, Sheena Cotter and Rebecca Kilner proposed to widen the definition of social immunity to "any type of immune response that has been selected to increase the fitness of the challenged individual and one or more recipients", and recommended that the phenomena described by Cremer be known as collective immunity.[5] This definition places importance on the evolutionary origin of behaviours rather than on their functional role at present; Cotter and Kilner explained that their broader definition would include immune behaviours in both animal families and social microbes as well as situations where herd immunity exists due to investment in personal immunity, arguing that this allowed for investigations of the evolution of social immunity to have a "greater depth than would otherwise be possible".[5] They further suggested that the evolution of social immunity be seen as one of the major transitions in evolution.[5] Joël Meunier proposed a further redefinition in his 2015 paper on the role of social immunity in the evolution of group living, suggesting that Cotter and Kilner's definition could problematically encompass immune defences which arise not due to social life but due to shared location; Meunier defines a social immune system as "any collective and personal mechanism that has emerged and/or is maintained at least partly due to the anti-parasite defence it provides to other group members".[1]

Mechanisms

Upon exposure to a parasite, group members must both evaluate the threat it poses and the current level of colony infection in order to respond appropriately. Mechanisms of social immunity are often categorized by the stage of the parasite attack on a group of organisms they target.

prophylactic (e.g. burying beetles smearing their carcasses with antimicrobials or termites fumigating their nests with naphthalene) whilst others are activated in response to a parasite challenge (e.g. imprisoning of parasitic beetles by honeybees or by the miniature 'hitchhiking' leafcutter ants who travel on larger workers' leaves to fight off parasitoid flies).[6]

In insects

For a parasite to succeed in infecting multiple members of an insect group, it must complete three key tasks:

  1. be taken up from the extra-nest environment into the nest
  2. establish itself within the nest
  3. multiply and spread to many more insect group members

Mechanisms of social immunity are thus often categorized by which step(s) they hinder and/or block.[1] Levels of sociality across the class

conspecific corpses from the nest or to isolate an infected group member - and yet these behaviours (and many more) have only been recorded in eusocial species.[1] Alternatively it may be the case that whilst the three conditions of eusociality themselves are not prerequisites for the emergence of these behaviours, secondary consequences of eusociality are. Perhaps the large number of individuals in eusocial colonies increases the efficiency of collective anti-parasite defences and thus their emergence begins to be selected for; or perhaps the preponderance of non-reproductive individuals is a necessary driver for the evolution of these behaviours, as when in a colony attacked by a parasite they can only increase their indirect fitness via social immunity directed at the queen's brood.[1]

The lack of collective defences in some eusocial taxa also shows that social immunity may also not always be adaptive (due to

Monomorium pharaonis) choose to move into infected nests over uninfected ones and queen wood ants (Formica paralugubris) are not repelled but actually attracted to habitats contaminated with entamopathogenic fungi.[1]

Inhibiting parasite uptake into the nest

Italian honeybees
(Apis mellifera ligustica)—the outward-facing bees are guarding the entrance

A parasite may be passively transported into a nest by a group member or may actively search for the nest; once inside, parasite transmission can be vertical (from mother to daughter colony into the next generation) or horizontally (between/within colonies).[2] In eusocial insects, the most frequent defence against parasite uptake into the nest is to prevent infection during and/or after foraging,[1] and a wide range of active and prophylactic mechanisms have evolved to this end.[1][2]

Atta
, one hitchhiking

Aversion to consuming or coming into contact with contaminated material also exists in presocial species, e.g., the gregarious-phase migratory grasshoppers Melanoplus sanguinipes avoids consuming conspecific corpses infected by entomoparasitic fungi. Female burying beetles (Nicrophorus vespilloides) choose fresh carcasses over microbe-covered degraded ones to breed on - though this may have also evolved to allow a reduction in post-hatching competition between juveniles and microbes over the carcass.[14]

It is currently unclear whether these aversive behaviours evolved and/or are maintained due to social interactions - the increase in direct fitness that avoiding contaminated material confers means that more research is required to tease out the indirect fitness benefits from the direct.[1]

Inhibiting the parasite establishing itself within the nest

Once a parasite has entered the nest, colonies must now prevent the establishment of the parasite - this is particularly important for long-lived societies which without would accrue a high parasite load.[2] In eusocial insects the most common mechanisms to stop establishment involve sanitising the nest and integrating substances with antimicrobial activity into nest material - nest hygiene behaviours.[1][2] Examples include:

  • In the ant lineage a unique antimicrobial
    Camponotus gigas
    ) carrying a dead conspecific
  • The corpses of group members killed by an infectious disease present a serious hazard to colony health (as in natural environments death from disease is much more common than death from old age): one mechanism that has evolved to help neutralize this risk is
    Apis mellifera): 1–2% of a colony are undertaker bees, specialized for corpse removal: they inspect corpses with their antennae before rapidly dropping them from the nest.[24][27]
  • Waste material is removed continuously and deposited in refuse piles as above (or even by some Atta ants into streams).
    faecal material promotes the growth of Actinomycetota with natural antimicrobial activity (e.g. Streptomyces), combating fungal parasites like M. anisopliae.[31] Colony members of the buff-tailed bumblebee (Bombus terrestris) defend themselves against the virulent Crithidia bombi parasite by consuming beneficial gut bacteria from the faces of conspecific after eclosing.[32]
    Small hive beetles inside a bee colony
  • Workers of the Cape honeybee (
    pronotum), honeybee workers find it difficult to decapitate and kill.[33] Instead, workers seal the small hive beetles in using 'bee glue' (propolis).[33] Construction of the 'propolis prisons' by some workers takes 1–4 days but is accompanied by other workers guarding the small hive beetle to prevent it escaping. Guards have been observed remaining day and night for up to 57 days and attacking the small hive beetle if it tried to escape.[33]

Some non-eusocial insects also sanitize their nests: the wood cockroach (Cryptocercus punctulatus) commonly defecates within the nest (this species nests in decaying wood, which often has a high microbe density), and faeces have been found to have antifungal activity against M. anisopliae, possibly mediated by microbes.[34] The galleries constructed within spruce trees by spruce beetles (Dendroctonus rufipennis) are under threat from multiple species of fungus which reduce spruce beetle fitness.[35] Upon fungal invasion, adults begin secreting orally and analysis of these secretions has revealed bacteria with antifungal activity; faecal pellets are used to quarantine off fungally-infested sections of the gallery.[35] A waste management strategy exists in some group living and subsocial species, such as the subsocial De Geer's short-tailed cricket (Anurogryllus muticus).[1] 5–10 minutes after defecating and returning to her eggs, A. muticus females return to the fecal pellets and removes them out of the chamber — note no other items are removed from the chamber.[36] Upon discovering a carcass, subsocial N. vespilloides parents upregulate the antimicrobial activity of their anal exudates and smear them over the carcass - thus sanitizing the resource their brood will soon feast on.[37]

Inhibiting intra-group transmission

If a parasite has entered the nest and established itself, groups must now mount defences which inhibit the spread of parasites from infected to uninfected group members.[2] The risk of infection for an uninfected individual is dependent on three factors: their susceptibility to the parasite, contact rate between infected and uninfected individuals and the infective ability (virulence) of the parasite.[2] In eusocial insects, defences include:

  • chitnolytic activity of labial gland secretions before being expelled as a pellet with other debris to refuse piles in or out of the nest.[2][38][39][40] Upon exposure to M. anisopliae, self-grooming rates of the dampwood termite Z. angusticollis remain constant whilst allogrooming increases by up to 53-fold; allogrooming here may not only remove fungal spores as the saliva applied concomitantly could reduce spore viability, similar to the antibacterial activity of Vespula wasp larvae's saliva.[41][42] Some honeybee workers become specialized for near-continuous allogrooming.[43]
  • Colony-level inhibitory strategies can also create 'organizational immunity'. For example, social insect workers tend to work initially at the centre of the nest, nursing the brood, and as they age adopt tasks closer and closer to the periphery, e.g., foraging.[44] This compartmentalization, termed centrifugal polyethism, means that workers of the same age interact mainly with others of the same age, who are performing the same task in the same spatial compartment: thus if a new disease arises that is transmitted through physical worker-worker contact it is limited to one section of the colony.[2] The spatial structuring of western honey bee colonies (Apis mellifera) privileges young individuals-when colonies are afflicted with diseases that have a short infectious period (the time period during which infected individuals can transmit the disease to susceptible individuals), it is confined only to the older individuals closer to the outside.[45] In the common eastern bumblebee (Bombus impatiens), workers who feed larvae tend to remain near the centre of the nest even when not performing this activity, and the converse is true for workers who forage; 11–13% of workers remain in small zones a particular distance from the nest centre throughout their life.[46] The demographic distribution of a colony can also can be utilized for antiparasite purposes: work on Z. angusticollis has shown that not only are there differences to parasite susceptibility between instars but that the demographic constitution of a group significantly affects survivorship (mixed age groups do better than single-age groups).[47] The effect of colony structuring on disease dynamics and social immunity is also analyzed theoretically using mathematical models.[48][49]
Dying Temnothorax unifasciatus workers voluntarily exclude themselves from the colony and die in solitude
  • Social exclusion of infected individuals can also prevent intra-group transmission. When dampwood termites (Z. angusticollis) come into contact with high densities of entamopathogenic fungal spores, they perform a whole-body "vibratory motor display" which induce others who are not in direct contact with the spores to flee, increasing their distance from the infected individual.[50] In the eastern subterranean termite (R. flavipes) infection with the same fungus also causes a vibratory alarm response; termites then aggregate around the infected individual and box it in, preventing it from moving to other areas of the colony; it is sometimes licked and bitten before subsequently being buried.[51] Individual Temnothorax unifasciatus ants who are dying due to fungal infection, carbon dioxide poisoning or 'naturally' (of unknown cause in colonies which had not been experimentally manipulated) permanently leave the nest one to 50 hours before their death, altruistically ceasing all social interactions with nestmates and dying alone away from the colony.[21] Some Apis mellifera workers are 'hygiene specialists'—they detect cells in the colony containing diseased or dead brood, uncap these cells and then remove the cell contents.[52]
  • The genetic homogeneity of insect colonies makes them theoretically susceptible to infection en masse; the high similarity of each group members genome means that each is susceptible (and resistant) to the same parasites,
    polyandry found in social insect colonies.[53][54] Social Hymenoptera also have exceptionally high rates of meiotic recombination when compared against a wide range of higher eukaryote taxa which further increases genetic diversity.[55] Ongoing theoretical and empirical work is seeking to tease out the scenarios in which these immune benefits of genetic heterogeneity can be negated due to concomitant costs, e.g., the increased intra-colony conflict and/or susceptibility to an increasing number of parasites which comes with increased genetic diversity.[56]
  • To combat heat-sensitive parasites, group members can elevate their temperature collectively—this defence is known as social fever and so far has only been found in honeybees (Apis):[1] upon challenge by chalk brood (Ascosphaera apis), workers increase nest temperature preventatively—it is currently undetermined whether the cue for this action is due to the larvae communicating their infection to the workers or the workers detecting the parasite before symptoms develop.[57]

Allogrooming exists in

presocial insects—the European earwig (Forficula auricularia) grooms its eggs to prevent mold growth[58] and wood roach (Cryptocercus) nymphs spend up to a fifth of their time grooming adults (nymphs also groom other nymphs but at a lower frequency, however allogrooming is not seen in adults)—[59] but overall the role of parasite defence in presocial taxa's allogrooming behaviour is currently unresolved.[1]

Nest abandonment is a last resort for a colony overwhelmed by an infection against which the defences listed above have not been effective—infected individuals can then be left deserted in the old nest or expelled from the group whilst the colony travels to a new nest.[2]

Leontopithecus rosalia
)

Other taxa

Social immune systems have been observed across a wide range of taxonomic groups. Allogrooming is found in many animals—for example

Parus caeruleus) prophylactically line their nest with aromatic plants (such as Achillea ligustica, Helichrysum italicum and Lavandula stoechas) to ward off mosquitoes and other blood-sucking ornithophillous (bird-targeting) insects.[64]

According to Richard Dawkins's concept of the extended phenotype, human healthcare activities, such as vaccination (depicted here) could be seen as social immunity

After the broader definition of social immunity by Cotter and Kilner, numerous examples of social immune behaviours within animal families can be given: túngara frogs (

blenny also use chemical strategies to defend their eggs from microbes.[5] Intriguingly, microbes themselves have been found to have social immune systems: when a population of Staphylococcus aureus is infected with gentamicin, some individuals (called small colony variants) begin to respire anaerobically, lowering the pH of the environment and thus conferring resistance to the antibiotic to all other individuals-including those S. aureus individuals who did not switch phenotype.[65] An analogy can be drawn here with the social fever in bees described above: a subset of individuals in a population change their behaviour and in doing so provide population-wide resistance.[5]

Using

extended phenotype, the healthcare systems developed by humans could be seen as a form of social immunity.[4]

Study species

The majority of studies on social immunity have been on eusocial insects.[1] For example, Sylvia Cremer's work uses ants as a model system whilst Rebeca Rosengaus works with termites. Outside of eusocial insects, one emerging model system is the burying beetle Nicrophorus vespilloides.[66]

Nicrophorus vespilloides

Two N. vespilloides preparing a carcass
Further information: Nicrophorus vespilloides

Already a

phenoloxidase activity decreases), and that the specifics of this social immune system differed between the sexes: female exudate has greater antibacterial activity than males; widowed males increased the antibacterial activity of their exudate whilst a reduction was seen in widowed females.[37]

Cotter et al. went on to show the costliness of this social immune response-by providing females with microbe-infested carcasses, they found that the upregulation of antibacterial activity that followed led to a 16% decrease in lifetime reproductive output.[67] This significant reduction in fitness, due to both increased mortality and age-related dropoff in fecundity, explains why the antibacterial activity of the exudate is only induced and not present constitutively.[67] Further work revealed how a trade-off existed between investment in personal immunity vs investment in social immunity, i.e., upon injury, N. vespilloides upregulates its personal immune response whilst concomitantly reducing its social immune response.[68] Recently, the Kilner Group identified a gene associated with social immunity in N. vespilloides: the expression rate of Lys6, a lysozyme, increases 1,409 times when breeding, and goes from the 5,967th most abundant transcript in the transcriptome of gut tissue to the 14th; it was also demonstrated that expression rates of Lys6 covary with the antibacterial activity of the anal exudate.[69] Social immunity efforts peaks during middle-age, in contrast to efforts in personal immunity increasing or being maintained with age in breeding burying beetles.[70]

The exudate of the larvae themselves also contains antibacterial substances, with activity peaking at hatching and declining as the larvae age. Rfemoving parents results in a downregulation of antibacterial effort, possibly due to the need to invest energy in other more important tasks that arise due to parental absence.[71]

Evolution

Comparison with personal immunity

Many researchers have noticed marked parallels between the more familiar personal immune systems of individual organisms (e.g. T and B lymphocytes) and the social immune systems described above, and it is generally appreciated among ecological immunologists that rigorous comparative work between these two systems will increase of understanding of the evolution of social immunity.[4][5] Whilst the specific physiological mechanisms by which immunity is produced differ sharply between the individual and society, it is thought that at a "phenomenological" level the principles of parasite threat and response are similar: parasites must be detected rapidly, responses should differ depending on the parasite in question, spread of the infection must be limited and different components of the individual/society should be afforded different levels of protection depending on their relative fitness contribution.[4] Cremer was the first to do this systematically, and partitioned immunological phenomena into three categories: border defence (intake avoidance), soma defence (avoid establishment within non-reproductive components of an individual/society) and germ-line defence (avoid infection of the reproductive components of an individual/society). Example analogies from Cremer's paper are:

  • Border defence:
    • Clotting in an individual's wounded blood vessels can be compared to the entrance-plugging behaviour of special ant workers in response to a parasite attack
    • The circulatory system of an individual can be compared to nutrient distribution in social insect colonies, where a few forage and then distribute it to the rest of the nest
    • Cats and dog self-grooming can be compared to allogrooming
  • Soma defence:
    • Granulomas form to contain diseases that individual immune systems are struggling to eliminate; this can be compared to the social encapsulation seen against small hive beetles in honeybees
    • Apoptosis in response to disease can be compared to the killing of infected workers or the enforced suicide seen in Temnothorax
  • Germ-line defence:
    • The special protection afforded to reproductive organs (e.g. blood-ovary/blood-testes barrier, increased number of immune cells relative to non-reproductive organs) can be compared to the royal chamber found in social insects, where due to centrifugal polyethism the queen(s), and sometimes king(s), are cared for by young workers who have remained inside the nest their whole life and thus have a lower probability of parasite infection

Other similarities include the immunological memory of the

brood parasitism and the worker policing behaviours which suppress 'social tumours'.[4] Specific immune cells in animals 'patrol' tissues looking for parasites, as do worker-caste individuals in colonies.[4]

Cotter and Kilner argue that not only is social immunity a useful concept to use when studying the major transitions in evolution (see below), that the origin of social immune systems might be considered a major transition itself.[5]

Role in the evolution of group living

The transition from solitary living to group living (identified by

S. gregaria express more genes involved in immunity than infected individuals in the gregarious phase,[78] Bombus terrestris workers also upregulate immune-related genes when experimentally isolated and there are three times more immune-related gene families in solitary insects than in the eusocial honeybees.[79]

Joël Meunier argued that the two seemingly contradictory relationships between personal immune effort and population density were a function of two assumptions implicit in the prediction that there should be a negative correlation between personal immune effort and group living:

  1. "Group living is always associated with the expression of social immunity" – this is false; worker termites (Z. angusticollis) do not discriminate between infected and uninfected conspecifics, pharaoh ant colonies (Monomorium pharaonis) choose to move into infected nests over uninfected ones and queen wood ant (Formica paralugubris) are not repelled but actually attracted to habitats contaminated with entamopathogenic fungi.[1]
  2. "Social immune responses are costly for producers" – only in one species, Nicrophorus vespilloides, has this assumption been tested[1] - a bacterial challenge to the larval resource led to a social immune response by the mother, and this response did lead to a reduction in lifetime reproductive success (i.e. there was a cost).[67]

Whilst advising that further studies in lots of different eusocial and non-eusocial taxa are required to better assess the validity of these assumptions, Meunier notes that the existence of a trade-off between personal and social immunity could be masked or erroneously 'discovered' in a population/species due to individual variation (e.g. low-quality individuals may not be able to afford relatively high investment into both immune systems), and thus recommends that the intrinsic quality of individuals should be controlled for if valid conclusions are to be drawn.[1]

To assess what current knowledge of social immune systems suggested about whether social immunity was a byproduct or driver of complex group living, Meunier delineated 30 different mechanisms of social immunity found in eusocial insects and looked for counterparts to these in presocial and solitary insects.[1] Supporting the hypothesis that social immunity was a driver and not a by-product of complex group living, ten mechanisms had counterparts in presocial insects and four in solitary species (though this does not imply that some mechanisms may evolve as a byproduct).[1] Evidence that social immunity mechanisms are selected for at least somewhat due to collective benefits is lacking though – possibly due to the difficulty in isolating the immune benefits from the other benefits that social immunity mechanisms often bestow (e.g. allogrooming inhibits the establishment of ectoparasites, but also improves the accuracy of nest mate recognition due to the sharing and thus homogenization of chemical signatures between group members), and the difficulty in experimentally separating direct fitness from indirect fitness, potentiated in eusocial taxa where sterile/non-reproductive individuals predominatee.[1] More studies on presocial taxa would allow for phyletic analyses to recover the actual path of evolution that different mechanisms of social immunity took.[1]

Role in the evolution of polyandry

The origin of

coefficient of relatedness is also important, as reducing the relatedness of workers limits the power of kin selection to maintain the ultracooperative behaviours which are vital to a colonies' success.[80][81] One hypothesis for the evolution of polyandry draws on the disease resistance that increased genetic diversity supposedly brings for a group, and a growing body of evidence from insect taxa supports this hypothesis, some of it discussed above.[80][82]

Concept

Levels of [null immunity] in societies. Each group member has its own individual immunity (ellipse) that comprises (i) its physiological immune system, which may involve either only the innate (I) immune component (e.g. as in invertebrates), or also an acquired (A) immune component (e.g. as in vertebrates), and (ii) its anti-parasite behaviours (B, dark grey). In social groups, the additional level of social immunity arises from the collective defences (pale grey, dotted line) of its group members, e.g. mutual sanitary care (arrows; adapted from Cremer & Sixt.[83]).

Social immunity is the

primates,[86] and has also been broadened to include other social interactions, such as parental care.[87] It is a recently developed concept.[88]

Schematic depicting the overlapping nature of the different components of collective disease defences.

Social immunity provides an integrated approach for the study of

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,

immune group, where pathogens are unable to spread due to the high ratio of immune to susceptible hosts.[84] 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.[90]

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

infectious diseases.[91] As social organisms are often densely aggregated and exhibit high levels of interaction, pathogens can more easily spread from infectious to susceptible individuals.[92] The intimate interactions often found in social insects, such as the sharing of food through regurgitation, are further possible routes of pathogen transmission.[88] As the members of social groups are typically closely related, they are more likely to be susceptible to the same pathogens.[93] 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.[93] In the case of species that live in nests/burrows, stable, homeostatic temperatures and humidity may create ideal conditions for pathogen growth.[93]

Disease risk is further affected by the

intraspecific pathogen transmission.[94][95]
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.

Components of social immunity in insect societies

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.

symptoms of the disease are expressed and can therefore be viewed as a preventative measure to avoid chalk brood outbreaks in the colony.[114]

Sanitary care of group members

Social insects conduct grooming to mechanically remove the infectious stages of pathogens (green dots) from the body surface of exposed group members (such as larvae) and apply antimicrobial chemicals, such as their formic acid rich poison, which inhibits pathogen growth.[115]

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

allogrooming (social grooming) to prevent infection. As conidia of such fungi only loosely attach to the cuticle of the host to begin with,[116] grooming can dramatically reduce the number of infective stages.[117][118] 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.[119][120][121][122]

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.[118] 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.[118] 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.[123]

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.

synergistically to inhibit conidia viability, by as much as 96%.[118]

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.[117][126][127] As mentioned above, dead nestmates are typically removed from the nest to reduce the potential risk of disease transmission.[112] Infected or not, ants that are close to death can also voluntarily remove themselves from the colony to limit this risk.[128][129] Honeybees can reduce social interactions with infected nest mates,[130] actively drag them out of the hive,[131] and may bar them from entering at all.[132] "Hygienic behaviour" is the specific removal of infected brood from the colony and has been reported in both honeybees and ants.[120][133] 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.[126] Cannibalism of infected nest mates is an effective behaviour in termites, as ingested infectious material is destroyed by antimicrobial enzymes present in their guts.[110][123][134] 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.[123] 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.[110] Some fungal pathogens (e.g. Ophiocordyceps, Pandora) manipulate their ant hosts into leaving the nest and climbing plant stems surrounding the colony.[135] There, attached to the stem, they die and rain down new spores onto healthy foragers.[136] To combat these fungi, healthy ants actively search for corpses on plant stems and attempt to remove them before they can release their spores[137]

Colony-level immunisation

dampwood termite-fungus system,[138] a garden ant-fungus system[139][140] and a carpenter ant–bacterium system.[141] 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 [140] and termite-fungus [142] 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[140]

Organisational defence

The controlled interactions between colony members through spatial, behavioural and temporal segregation, is thought to restrict disease transmission.

Organisational disease defence — or organisational immunity — refers to patterns of social interactions which could, hypothetically, mitigate disease transmission in a social group.

interaction networks upon disease coming into the colony. However, the organisational immunity hypothesis is currently mainly supported by theoretical models and awaits empirical testing.[90]

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External links
Retrieved from "https://en.wikipedia.org/w/index.php?title=Social_immunity&oldid=1195832141"