Social immunity is any antiparasite defence mounted for the benefit of individuals other than the actor. For parasites, the frequent contact, high population density and low genetic variability makes social groups of organisms a promising target for infection: this has driven the evolution of collective and cooperative anti-parasite mechanisms that both prevent the establishment of and reduce the damage of diseases among group members. Social immune mechanisms range from the prophylactic, such as burying beetles smearing their carcasses with antimicrobials or termites fumigating their nests with naphthalene, to the active defenses seen in the imprisoning of parasitic beetles by honeybees or by the miniature 'hitchhiking' leafcutter ants which travel on larger worker's leaves to fight off parasitoid flies. Whilst many specific social immune mechanisms had been studied in relative isolation (e.g. the "collective medication" of wood ants), it was not until Sylvia Cremer et al.'s 2007 paper "Social Immunity" that the topic was seriously considered. Empirical and theoretical work in social immunity continues to reveal not only new mechanisms of protection but also implications for understanding of the evolution of group living and polyandry.
Social immunity (also termed collective immunity) describes the additional level of disease protection arising in social groups from collective disease defences, performed either jointly or towards one another. These collective defences complement the individual immunity of all group members and constitute an extra layer of protection at the group level, combining behavioural, physiological and organisational adaptations. These defences can be employed either prophylactically or on demand.
Definition
Sylvia Cremer defined social immunity in her seminal 2007 Current Biology paper "Social Immunity" as the "collective action or altruistic behaviours of infected individuals that benefit the colony". She laid out a conceptual framework for the topic using examples from primates and eusocial insects. Cremer's definition focused on the collective benefits of behaviours and was adopted by other behavioural ecologists (e.g. Wilson-Rich 2009) when describing immune phenomena which were contingent on the action of multiple individuals. 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". 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. 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". They further suggested that the evolution of social immunity be seen as one of the major transitions in evolution. 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".
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. Some mechanisms are 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).
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 they hinder and/or block. Levels of sociality across the class Insecta range from eusocial species (with cooperative brood care, overlapping generations within a colony of adults and a division of labour into reproductive and non-reproductive castes) to solitary living, with many intermediate systems in between which despite lacking full eusociality still may exhibit parental care or nest cohabitation. Different systems of social organization alter both the possibility and cost-benefit ratio of social immune mechanisms (e.g. guarding the entrance to the nest requires both division of labour, whilst allogrooming merely requires behavioural interactions), though the absence of many behaviours currently only recorded in eusocial taxa from non-eusocial taxa may simply be due to a lack of study of these group's social immune systems. For instance it seems plausible that insects living in common nest sites could evolve to remove 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. 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.
The lack of collective defences in some eusocial taxa also shows that social immunity may also not always be adaptive (due to life history costs or ineffectiveness against a particular parasite's infective strategy), and that living in a group does not necessitate the expression of any particular suite of social immunity mechanisms. For example, worker termites (Zootermopsiss 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 ants (Formica paralugubris) are not repelled but actually attracted to habitats contaminated with entomopathogenic fungi.
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). In eusocial insects, the most frequent defence against parasite uptake into the nest is to prevent infection during and/or after foraging, and a wide range of active and prophylactic mechanisms have evolved to this end.
Nest guards of honeybees (Apis) guard the nest not just from predators, but from parasites as well— bees infected with hairless-black syndrome are attacked by healthy honeybees which chew vigorously with their mandibles all over the infected bee's exoskeleton. 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). Bees infected with chronic bee paralysis are subject to a higher level of aggressive behaviours than intruders or hivemates. Workers of the tropical leafcutter ant bringing leaf fragments back to the nest are at risk of attack by parasitiodic phorid flies, who often land on leaf fragments and then proceed to oviposit (egg-lay) into the ant's head. To help combat this, small workers (minims) in at least seven species of Atta hitchhike on the leaves, deterring parasitoid attack. 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. Individual foragers can also avoid picking up parasites by avoiding contaminated habitats, such as the subterranean termite Reticulitermes tibialis which avoids food sources contaminated with the entomogenous nematode Steinernema feltiae. Another termite, Macrotermes michaelseni, avoids the entompathogenic fungi Metarhizium anisopliae and Beauveria bassiana and repellence is positively correlated with the virulence of the particular fungus (very virulent fungi also induce avoidance at some distance away). 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 entomopathogenic bacteria and thus avoid infected corpses; R. tibalis does not cannibalize conspecifics infected with M. anisopliae. 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.
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.
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. 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. Examples include: