Social immunity
Social immunity is any antiparasite defence mounted for the benefit of individuals other than the actor. For
Social immunity (also termed collective immunity) describes the additional level of disease protection arising in social groups from collective
Definition
Sylvia Cremer defined social immunity in her seminal 2007 Current Biology paper 'Social Immunity' as the "collective action or
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.
In insects
For a parasite to succeed in infecting multiple members of an insect group, it must complete three key tasks:
- be taken up from the extra-nest environment into the nest
- establish itself within the nest
- 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
The lack of collective defences in some eusocial taxa also shows that social immunity may also not always be adaptive (due to
Inhibiting parasite uptake into the nest
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]
- Nest guards of honeybees (Apis) guard the nest not just from predators, but from parasites as well—[1][2] bees infected with hairless-black syndrome are attacked by healthy honeybees which chew vigorously with their mandibles all over the infected bee's exoskeleton.[7] In one study, attacks lasted up to 478 seconds (average of 62 seconds) with overall levels of attack behaviour cycling (highest levels between 12:00 and 16:00 each day, peaking every 4–12 days).[7] Bees infected with chronic bee paralysis are subject to a higher level of aggressive behaviours than intruders or hivemates.[8]
- Workers of the tropical Atta hitchhike on the leaves, deterring parasitoid attack.[6] Many possible additional functions of hitchhiking have been proposed, some pertinent to social immunity; evidence exists that the primary function of hitchhiking minims' is actually to inspect and clean the leaf fragments prior to their entry into the colony, removing microbial parasites and contaminants.[6]
- Individual foragers can also avoid picking up parasites by avoiding contaminated habitats, such as the subterranean termite Metarhizium anisopliae and Beauveria bassian and repellence is positively correlated with the virulence of the particular fungus (very virulent fungi also induce avoidance at some distance away).[11]
- Similarly, individuals can inhibit parasite uptake by refraining from consuming infected conspecifics. Argentine ants (Linepithema humile) and cornfield ants (Lasius alienus) both detect chemical 'ant deterrent factors' adaptively produced by entamopathogenic bacteria and thus avoid infected corpses;[12] R. tibalis does not cannibalize conspecifics infected with M. anisopliae.[13]
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
- 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]
- 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
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]
Other taxa
Social immune systems have been observed across a wide range of taxonomic groups. Allogrooming is found in many animals—for example
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 (
Using
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
Already a
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
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
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:
- "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]
- "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
Concept
Social immunity is the
Social immunity provides an integrated approach for the study of
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,
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
Disease risk is further affected by the
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.
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
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.
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
Organisational defence
Organisational disease defence — or organisational immunity — refers to patterns of social interactions which could, hypothetically, mitigate disease transmission in a social group.
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