Social immunity

Giant Moray Eel getting cleaned.jpg 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 which is 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 napthalene, 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 parasitioid flies. Whilst many specific social immune mechanisms have been studied for some time in relative isolation (e.g. the "collective medication" found in wood ants), it was only until Sylvia Cremer et al.'s 2007 landmark paper 'Social Immunity' in Current Biology did the topic become seriously considered as a whole, conceptually and in an evolutionary sense. Empirical and theoretical work in social immunity continues to reveal not only new mechanisms of protection but also implications for our understanding of the evolution of group living and polyandry, as well as having consequences for our more general understanding of the origin of complex regulatory systems.

Definition

Sylvia Cremer (then at the University of Regensburg) gave the first definition of social immunity in her seminal 2007 Current Biology paper 'Social Immunity', saying that the "collective action or altruistic behaviours of infected individuals that benefit the colony" before laying out a conceptual framework for thinking about the topic using examples from primates and 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 (both then at the University of Cambridge) 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 (University of Mainz) 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.[1] Some mechanisms are prophylactic (e.g. burying beetles smearing their carcasses with antimicrobials or termites fumigating their nests with napthalene) 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 parasitioid flies).[6]

In insects

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

  1. The parasite must be taken up from the extra-nest environment into the nest
  2. The parasite must establish itself within the nest
  3. The parasite must 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 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.[1] 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.[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 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 entamopathogenic fungi.[1]

Inhibiting parasite uptake into the nest

The entrance to a hive of 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]

Two leafcutter ants of the genus 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:

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 anitmicrobial 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:

Dying Temnothorax unifasciatus workers voluntarily exclude themselves from the colony and die in solitude

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]

Allogrooming in golden lion tamarins (Leontopithecus rosalia)

Other taxa

Whilst most studies of social immunity have focused on eusocial insects, social immune systems have been observed across a wide range of taxonomic groups. Allogrooming is found in many animals—for example primates frequently groom others, a behaviour which likely evolved for its hygienic function but has now been co-opted for its additional role in social bonding.[60] Allogrooming in the common vampire bat (Desmodus rotundus) is associated with the regurgitation of food and may allow other bats to identify which individuals are capable of supplying them with food;[61] the allogrooming behaviours of horses and birds have also been the focus of research.[62][63] A range of sometimes elaborate cleaning symbioses also exist between many different species, especially in marine fish with their cleaning stations. Corsican blue tits (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' 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 (Engystomops pustulosus) create 'foam nests' during breeding in which embryogenesis occurs; these foam nests are imbued with ranaspumin proteins which provide defence against microbial attack and act as a detergent. The three-spined stickleback (Gasterosteus aculeatus), grass goby (Zosterisessor ophiocephalus), fringed darter (Etheostoma crossopterum) and two species of 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 Richard Dawkins concept of the 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 are carried out on eusocial insects[1], e.g. Sylvia Cremer's work uses ants as a model system whilst Rebeca Rosengaus (Northeastern University) works with termites. Outside of eusocial insects, one emerging model system is the burying beetle Nicrophorus vespilloides[66] and is discussed as an example of the study of social immunity below.

Nicrophorus vespilloides

Two N. vespilloides preparing a carcass

Already a model system in evolutionary ecology due to their extensive parental care, burying beetles like N. vespilloides hunt for small vertebrate carcasses which they then bury before intricately preparing it as a resource for its larvae to breed on-these carcasses are scarce and ephemeral yet are necessary for burying beetles' reproductive success. Carcasses are highly contested resources with challenges being launched by other burying beetles and other scavenging species, as well as microbial decomposers. Older carcasses have a higher microbial load and thus have a lower quality as a breeding resource: larvae raised on these carcasses are smaller and in a worse nutritional state–at adulthood these beetles were also smaller, which in N. vespilloides reduces fitness.[14] Daniel Rozen et al. demonstrated in 2008 that N. vespilloides preferentially chooses newer carcasses (which tend to have a lower microbial load) over old carcasses, and if it is not possible to acquire one of these higher quality carcasses that they use pre and post-hatching parental care to reduce the challenge posed by microbes.[14] Sheena Cotter and Rebecca Kilner demonstrated that part of this anti-microbial parental care involved both parents smearing the carcass with antibacterial anal exudates: their 2009 work demonstrated that when beetles encounter a carcass they upregulate the antibacterial activity of their anal exudate by actively altering its composition (lysozyme-like activity increases, 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 at the University of Cambridge's Department of Zoology 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 given below:

Other similarities include the immunological memory of the adaptive immune system in vertebrates and the observation that a similar collective memory (operating with a yet-to-be-explained mechanism) occurs in some insect societies e.g. individual Z. angusticollis survive M. anisopliae infections significantly more when they have been in contact with a previously infected conspecifc, a 'social transfer of immunity' or 'social vaccination'.[4][72] Transplant rejection caused by non-self major histocompatibility complexes is frequently thought to be a byproduct with no evolutionary function, however Cremer cites cases (such as the colonial star ascidian (Botryllus schlosseri)) where recognizing foreign cells may have evolved as an adaptation - if so, then this could be analogous to the self-recognition systems in social insects which prevent 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 John Maynard Smith as one of the seven major transitions in evolutionary history) brought with it many fitness benefits (increased anti-predator vigilance, foraging benefits etc.) and the opportunity to exploit a vast array of new ecological niches, but group living also has its pitfalls.[2][73] Numerous studies have demonstrated an increase in contact-transmitted parasite load with group size increase,[1][73] and thus research has been done on the role of social immunity in the evolution of early group living. Empirical evidence already exists, from both interspecific and intraspecific comparative studies, that an increase in population density drives an increase in personal immune effort (density-dependent prophylaxis).[74][75][76] However, there is also good evidence that the evolution of social immunity leads to a trade-off between effort into personal immune responses vs. effort in social immune responses - physiological and genomic studies have shown that social conditions can lead to a reduction in personal immune effort.[1] Personal immunity in the Australian plague locust (Chortoicetes terminifera) decreases upon an increase in population density and increases when artificially isolated.[77] Genomic studies reveal that infected solitary S. gregaria express more genes involved in immunity than infected individuals in the gregarious phase,[78] Bombus terrestris workers also upregualte 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 (University of Mainz) 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 bypoduct 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, 10 mechanisms had counterparts in presocial insects and 4 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 polyandry in nature and its adaptive value is a subject of ongoing controversy in evolutionary biology, partly due to the seemingly numerous costs it places on females - additional energetic and temporal allocation to reproduction, increased risk of predation, increased risk of sexually transmitted diseases and increased risk of physical harm caused by copulation/sexual coercion – for eusocial insects, the effects polyandry has on the colony member's 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]

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