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{{Afd-merge to|Social immunity|Social Immunity|18 February 2018}}
#redirect [[Social immunity]]
{{Orphan|date=November 2016}}
[[File:Lasius_neglectus_grooming.jpg|thumb|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. ]]
'''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.<ref name=cremer /> These collective defences complement the individual [[Immunity (medical)|immunity]] of all group members and constitute an extra layer of protection at the group level, combining [[Ethology|behavioural]], [[Physiology|physiological]] and organisational adaptations. These defences can be employed either [[Prophylaxis|prophylactically]] or on demand.

==Concept==
[[File:Immune modules 2.pdf|thumb|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 immune system|innate]] (I) immune component (e.g. as in [[invertebrate]]s), or also an [[Adaptive immune system|acquired]] (A) immune component (e.g. as in [[vertebrate]]s), and (ii) its anti-parasite [[Behavior|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.<ref name= "sixt">{{cite journal|last1=Cremer|first1=S.|last2=Sixt|first2=M.|title=Analogies in the evolution of individual and social immunity|journal=Philosophical Transactions of the Royal Society B: Biological Sciences|date=12 January 2009|volume=364|issue=1513|pages=129–142|doi=10.1098/rstb.2008.0166|pmid=18926974|pmc=2666697}}</ref>).]]
Social immunity is a recently developed concept<ref name="cremer" /> used to describe the [[evolution]] of an additional level of immunity in the colonies of [[eusocial]] insects (some [[bee]]s and [[wasps]], all [[ants]] and [[termites]]).<ref name=sixt /><ref name="masri" /><ref name=wilson>{{cite journal|last1=Wilson-Rich|first1=Noah|last2=Spivak|first2=Marla|last3=Fefferman|first3=Nina H.|last4=Starks|first4=Philip T.|title=Genetic, Individual, and Group Facilitation of Disease Resistance in Insect Societies|journal=Annual Review of Entomology|date=January 2009|volume=54|issue=1|pages=405–423|doi=10.1146/annurev.ento.53.103106.093301|pmid=18793100}}</ref> It is equally used to describe collective disease defences in other stable societies, including those of [[primates]],<ref>{{cite book|last1=Altizer|first1=Charles L. Nunn, Sonia|title=Infectious diseases in primates : behavior, ecology and evolution|date=2006|publisher=Oxford University Press|location=Oxford|isbn=978-0-19-856585-7|edition=[Online-Ausg.].}}</ref> and, has also been broadened to include other social interactions, such as [[parental care]].<ref>{{cite journal|last1=Cotter|first1=S. C.|last2=Kilner|first2=R. M.|title=Personal immunity versus social immunity|journal=Behavioral Ecology|date=4 June 2010|volume=21|issue=4|pages=663–668|doi=10.1093/beheco/arq070}}</ref>
[[File:Trinity of social immunity 2.pdf|thumb|left|Schematic depicting the overlapping nature of the different components of collective disease defences.]]
Social immunity provides an integrated approach for the study of [[disease]] dynamics in societies, combining both the behaviour and physiology (including molecular-level processes) of all group members and their social interactions. It thereby links the fields of [[social evolution]] and [[ecological immunology]]. Social immunity also affects [[epidemiology]], as it can impact both the course of an infection at the individual level, as well as the spread of disease within the group.

Social immunity differs from similar phenomena that can occur in groups that are not truly social (e.g. herding animals). These include (i) density dependent prophylaxis,<ref>{{cite journal|last1=WILSON|first1=KENNETH|last2=REESON|first2=ANDREW F.|title=Density-dependent prophylaxis: evidence from Lepidoptera–baculovirus interactions?|journal=Ecological Entomology|date=February 1998|volume=23|issue=1|pages=100–101|doi=10.1046/j.1365-2311.1998.00107.x}}</ref> which is the up regulation of the individual immunity of group members under temporal crowding, and (ii) [[herd immunity]], which is the protection of [[susceptible individual]]s in an otherwise [[immune]] group, where pathogens are unable to spread due to the high ratio of immune to susceptible hosts.<ref name=masri>{{cite journal|last1=Masri|first1=Leila|last2=Cremer|first2=Sylvia|title=Individual and social immunisation in insects|journal=Trends in Immunology|date=October 2014|volume=35|issue=10|pages=471–482|doi=10.1016/j.it.2014.08.005}}</ref> 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.<ref name=babz>{{cite journal|last1=Stroeymeyt|first1=Nathalie|last2=Casillas-Pérez|first2=Barbara|last3=Cremer|first3=Sylvia|title=Organisational immunity in social insects|journal=Current Opinion in Insect Science|date=November 2014|volume=5|pages=1–15|doi=10.1016/j.cois.2014.09.001}}</ref>

==Disease risk in social groups==
Sociality, although a very successful way of life, is thought to increase the per-individual risk of acquiring disease, simply because close contact with [[conspecifics]] is a key transmission route for [[infectious diseases]].<ref>{{cite journal|last1=Alexander|first1=R D|title=The Evolution of Social Behavior|journal=Annual Review of Ecology and Systematics|date=November 1974|volume=5|issue=1|pages=325–383|doi=10.1146/annurev.es.05.110174.001545}}</ref> As social organisms are often densely aggregated and exhibit high levels of interaction, pathogens can more easily spread from infectious to susceptible individuals.<ref>{{cite book|last1=Krause|first1=J|last2=Ruxton|first2=G D|title=Living in Groups|date=2002|publisher=Oxford University Press|location=New York|edition=1}}</ref> The intimate interactions often found in social insects, such as the sharing of food through regurgitation, are further possible routes of pathogen transmission.<ref name ="cremer">{{cite journal|last1=Cremer|first1=Sylvia|last2=Armitage|first2=Sophie A.O.|last3=Schmid-Hempel|first3=Paul|title=Social Immunity|journal=Current Biology|date=August 2007|volume=17|issue=16|pages=R693–R702|doi=10.1016/j.cub.2007.06.008}}</ref> As the members of social groups are typically closely related, they are more likely to be susceptible to the same pathogens.<ref name ="hempel">{{cite book|last1=Schmid-Hempel|first1=Paul|title=Parasites in Social Insects|date=1998|publisher=Princeton University Press|location=Princeton, New Jersey}}</ref> 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.<ref name="hempel" /> In the case of species that live in nests/burrows, stable, homeostatic temperatures and humidity may create ideal conditions for pathogen growth.<ref name="hempel" />

Disease risk is further affected by the [[ecology]]. For example, many social insects nest and forage in habitats that are rich in pathogens, such as soil or rotting wood, exposing them to a plethora of [[microparasites]], e.g. [[fungi]], [[bacteria]], [[viruses]] and [[macroparasites]], e.g. [[mites]] and [[nematode]]s.<ref name="hempel" /> In addition, shared food resources, such as flowers, can act as disease hubs for social insect [[pollinators]], promoting both [[interspecific]] and [[intraspecific]] pathogen transmission.<ref>{{cite journal|last1=McArt|first1=Scott H.|last2=Koch|first2=Hauke|last3=Irwin|first3=Rebecca E.|last4=Adler|first4=Lynn S.|last5=Gurevitch|first5=Jessica|title=Arranging the bouquet of disease: floral traits and the transmission of plant and animal pathogens|journal=Ecology Letters|date=May 2014|volume=17|issue=5|pages=624–636|doi=10.1111/ele.12257}}</ref><ref>{{cite journal|last1=Singh|first1=Rajwinder|last2=Levitt|first2=Abby L.|last3=Rajotte|first3=Edwin G.|last4=Holmes|first4=Edward C.|last5=Ostiguy|first5=Nancy|last6=vanEngelsdorp|first6=Dennis|last7=Lipkin|first7=W. Ian|last8=dePamphilis|first8=Claude W.|last9=Toth|first9=Amy L.|last10=Cox-Foster|first10=Diana L.|last11=Traveset|first11=Anna|title=RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmission via Pollen and Potential Impact on Non-Apis Hymenopteran Species|journal=PLoS ONE|date=22 December 2010|volume=5|issue=12|pages=e14357|doi=10.1371/journal.pone.0014357|pmid=21203504|pmc=3008715}}</ref> 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.<ref name=cremer /> Such behaviours can be employed either [[prophylactically]], or actively, upon demand. For example, social insects can incorporate materials with antimicrobial properties into their nest, such as conifer [[resin]],<ref>{{cite journal|last1=Christe|first1=Philippe|last2=Oppliger|first2=Anne|last3=Bancalà|first3=Francesco|last4=Castella|first4=Grégoire|last5=Chapuisat|first5=Michel|title=Evidence for collective medication in ants|journal=Ecology Letters|date=13 December 2002|volume=6|issue=1|pages=19–22|doi=10.1046/j.1461-0248.2003.00395.x}}</ref><ref>{{cite journal|last1=CASTELLA|first1=GRÉGOIRE|last2=CHAPUISAT|first2=MICHEL|last3=MORET|first3=YANNICK|last4=CHRISTE|first4=PHILIPPE|title=The presence of conifer resin decreases the use of the immune system in wood ants|journal=Ecological Entomology|date=June 2008|volume=33|issue=3|pages=408–412|doi=10.1111/j.1365-2311.2007.00983.x}}</ref> or faecal pellets that contain [[symbiont]] derived [[antimicrobials]].<ref>{{cite journal|last1=Rosengaus|first1=Rebeca B.|last2=Guldin|first2=Matthew R.|last3=Traniello|first3=James F. A.|title=Inhibitory effect of termite fecal pellets on fungal spore germination|journal=Journal of Chemical Ecology|date=1998|volume=24|issue=10|pages=1697–1706|doi=10.1023/A:1020872729671}}</ref><ref>{{cite journal|last1=Rosengaus|first1=Rebeca B.|last2=Mead|first2=Kerry|last3=Du Comb|first3=William S.|last4=Benson|first4=Ryan W.|last5=Godoy|first5=Veronica G.|title=Nest sanitation through [[defecation]]: antifungal properties of wood cockroach feces|journal=Naturwissenschaften|date=23 November 2013|volume=100|issue=11|pages=1051–1059|doi=10.1007/s00114-013-1110-x|pmid=24271031}}</ref><ref name ="rosen">{{cite journal|last1=Rosengaus|first1=Rebeca B.|last2=Schultheis|first2=Kelley F.|last3=Yalonetskaya|first3=Alla|last4=Bulmer|first4=Mark S.|last5=DuComb|first5=William S.|last6=Benson|first6=Ryan W.|last7=Thottam|first7=John P.|last8=Godoy-Carter|first8=Veronica|title=Symbiont-derived β-1,3-glucanases in a social insect: mutualism beyond nutrition|journal=Frontiers in Microbiology|date=21 November 2014|volume=5|doi=10.3389/fmicb.2014.00607}}</ref><ref>{{cite journal|last1=Chouvenc|first1=T.|last2=Efstathion|first2=C. A.|last3=Elliott|first3=M. L.|last4=Su|first4=N.-Y.|title=Extended disease resistance emerging from the faecal nest of a subterranean termite|journal=Proceedings of the Royal Society B: Biological Sciences|date=18 September 2013|volume=280|issue=1770|pages=20131885–20131885|doi=10.1098/rspb.2013.1885|pmid=24048157|pmc=3779336}}</ref> These materials reduce the growth and density of many detrimental bacteria and fungi. Antimicrobial substances can also be self-produced. Secretions from the metapleural glands of ants and volatile chemical components produced by termites have been shown to inhibit fungal germination and growth.<ref>{{cite journal|last1=Tranter|first1=C.|last2=Graystock|first2=P.|last3=Shaw|first3=C.|last4=Lopes|first4=J. F. S.|last5=Hughes|first5=W. O. H.|title=Sanitizing the fortress: protection of ant brood and nest material by worker antibiotics|journal=Behavioral Ecology and Sociobiology|date=13 December 2013|volume=68|issue=3|pages=499–507|doi=10.1007/s00265-013-1664-9}}</ref><ref>{{cite journal|last1=Poulsen|first1=Michael|last2=Bot|first2=Adrianne|last3=Nielsen|first3=Mogens|last4=Boomsma|first4=Jacobus|title=Experimental evidence for the costs and hygienic significance of the antibiotic metapleural gland secretion in leaf-cutting ants|journal=Behavioral Ecology and Sociobiology|date=1 July 2002|volume=52|issue=2|pages=151–157|doi=10.1007/s00265-002-0489-8}}</ref><ref>{{cite journal|last1=Ortius-Lechner|first1=Diethe|last2=Maile|first2=Roland|last3=Morgan|first3=E. David|last4=Boomsma|first4=Jacobus J.|title=Metapleural Gland Secretion of the Leaf-cutter Ant Acromyrmex octospinosus: New Compounds and Their Functional Significance|journal=Journal of Chemical Ecology|date=2000|volume=26|issue=7|pages=1667–1683|doi=10.1023/A:1005543030518}}</ref><ref>{{cite journal|last1=Chen|first1=J.|last2=Henderson|first2=G.|last3=Grimm|first3=C. C.|last4=Lloyd|first4=S. W.|last5=Laine|first5=R. A.|title=Termites fumigate their nests with naphthalene|journal=Nature|date=9 April 1998|volume=392|issue=6676|pages=558–559|doi=10.1038/33305}}</ref><ref>{{cite journal|last1=Matsuura|first1=Kenji|last2=Matsunaga|first2=Takeshi|title=Antifungal activity of a termite queen pheromone against egg-mimicking termite ball fungi|journal=Ecological Research|date=15 November 2014|volume=30|issue=1|pages=93–100|doi=10.1007/s11284-014-1213-7}}</ref> Another important component of nest hygiene is waste management, which involves strict spatial separation of clean nest areas and waste dumps.<ref name=cremer /> Social insect colonies often deposit their waste outside of the nest, or in special compartments, including waste chambers for food leftovers, “toilets” for defecation<ref>{{cite journal|last1=Czaczkes|first1=Tomer J.|last2=Heinze|first2=Jürgen|last3=Ruther|first3=Joachim|last4=d'Ettorre|first4=Patrizia|title=Nest Etiquette—Where Ants Go When Nature Calls|journal=PLOS ONE|date=18 February 2015|volume=10|issue=2|pages=e0118376|doi=10.1371/journal.pone.0118376|pmid=25692971|pmc=4332866}}</ref> and “graveyards”, where dead individuals are deposited, reducing the probability of parasite transmission from potentially infected [[cadavers]].<ref>{{cite journal|last1=Wilson|first1=E. O.|last2=Durlach|first2=N. I.|last3=Roth|first3=L. M.|title=Chemical Releaser of Necrophoric Behavior in Ants|journal=Psyche: A Journal of Entomology|date=1958|volume=65|issue=4|pages=108–114|doi=10.1155/1958/69391}}</ref><ref>{{cite journal|last1=Visscher|first1=P. Kirk|title=The honey bee way of death: Necrophoric behaviour in Apis mellifera colonies|journal=Animal Behaviour|date=November 1983|volume=31|issue=4|pages=1070–1076|doi=10.1016/S0003-3472(83)80014-1}}</ref><ref name="ReferenceA">{{cite journal|last1=Chouvenc|first1=Thomas|last2=Su|first2=Nan-Yao|last3=Hughes|first3=William|title=When Subterranean Termites Challenge the Rules of Fungal Epizootics|journal=PLoS ONE|date=28 March 2012|volume=7|issue=3|pages=e34484|doi=10.1371/journal.pone.0034484|pmid=22470575|pmc=3314638}}</ref><ref>{{cite journal|last1=Diez|first1=Lise|last2=Deneubourg|first2=Jean-Louis|last3=Detrain|first3=Claire|title=Social prophylaxis through distant corpse removal in ants|journal=Naturwissenschaften|date=7 September 2012|volume=99|issue=10|pages=833–842|doi=10.1007/s00114-012-0965-6|pmid=22955492}}</ref><ref name="ReferenceB">{{cite journal|last1=Sun|first1=Qian|last2=Zhou|first2=Xuguo|title=Corpse Management in Social Insects|journal=International Journal of Biological Sciences|date=2013|volume=9|issue=3|pages=313–321|doi=10.7150/ijbs.5781|pmid=23569436|pmc=3619097}}</ref> Where social insects place their waste is also important. For example, leaf cutting ants living in xeric conditions deposit their waste outside the nest, whilst species living in the tropics tend to keep it in special chambers within the nest. It has been proposed that this difference is related to the likelihood that the external environment reduces or enhances microbial growth.<ref>{{cite journal|last1=Farji-Brener|first1=Alejandro G.|last2=Elizalde|first2=Luciana|last3=Fernández-Marín|first3=Hermógenes|last4=Amador-Vargas|first4=Sabrina|title=Social life and sanitary risks: evolutionary and current ecological conditions determine waste management in leaf-cutting ants|journal=Proceedings of the Royal Society B: Biological Sciences|date=25 May 2016|volume=283|issue=1831|pages=20160625|doi=10.1098/rspb.2016.0625|pmid=27226469|pmc=4892804}}</ref> For xeric-living ants, placing waste outside will tend to inhibit infectious material, as microbes are usually killed under hot, dry conditions. On the other hand, placing waste into warm, humid environments will promote microbial growth and disease transmission, so it may be safer for ants living in the topics to contain their waste within the nest. [[Honeybees]] have evolved the ability to actively maintain a constant temperature within their hives to ensure optimal brood development. Upon exposure to ''Ascoshpaera apis'', a heat sensitive fungal pathogen that causes chalk brood, honeybees increase the temperature of the brood combs, thereby creating conditions that disfavour the growth of the pathogen. This "social fever" is performed before [[symptoms]] of the disease are expressed and can therefore be viewed as a preventative measure to avoid chalk brood outbreaks in the colony.<ref>{{cite journal|last1=Starks|first1=P. T.|last2=Blackie|first2=Caroline A.|last3=Seeley|first3=Thomas D.|title=Fever in honeybee colonies|journal=Naturwissenschaften|date=23 May 2000|volume=87|issue=5|pages=229–231|doi=10.1007/s001140050709|pmid=10883439}}</ref>

===Sanitary care of group members===
[[File:Ants_conducting_brood_grooming.pdf|thumb|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.<ref>{{Cite journal|last=Tragust|first=Simon|last2=Mitteregger|first2=Barbara|last3=Barone|first3=Vanessa|last4=Konrad|first4=Matthias|last5=Ugelvig|first5=Line V.|last6=Cremer|first6=Sylvia|title=Ants Disinfect Fungus-Exposed Brood by Oral Uptake and Spread of Their Poison|url=http://linkinghub.elsevier.com/retrieve/pii/S0960982212013784|journal=Current Biology|volume=23|issue=1|pages=76–82|doi=10.1016/j.cub.2012.11.034|pmid=23246409}}</ref>]]
Sanitary care reduces the risk of infection for group members and can slow the course of disease. For example, grooming is the first line of defence against externally-infected pathogens such as [[entomopathogenic fungi]], whose infectious [[conidia]] can be mechanically removed through self- and [[allogrooming]] (social grooming) to prevent infection. As conidia of such fungi only loosely attach to the cuticle of the host to begin with,<ref>{{cite book|last1=Deacon|first1=J W|title=Fungal Biology|date=2005|publisher=Blackwell Publishing|location=Oxford, UK|isbn=9781405130660|edition=4th}}</ref> grooming can dramatically reduce the number of infective stages.<ref name="Royal Society B 2002">{{cite journal|last1=Hughes|first1=W. O. H.|last2=Eilenberg|first2=J.|last3=Boomsma|first3=J. J.|title=Trade-offs in group living: transmission and disease resistance in leaf-cutting ants|journal=Proceedings of the Royal Society B: Biological Sciences|date=7 September 2002|volume=269|issue=1502|pages=1811–1819|doi=10.1098/rspb.2002.2113|pmid=12350269|pmc=1691100}}</ref><ref name= "tragust">{{cite journal|last1=Tragust|first1=Simon|last2=Mitteregger|first2=Barbara|last3=Barone|first3=Vanessa|last4=Konrad|first4=Matthias|last5=Ugelvig|first5=Line V.|last6=Cremer|first6=Sylvia|title=Ants Disinfect Fungus-Exposed Brood by Oral Uptake and Spread of Their Poison|journal=Current Biology|date=January 2013|volume=23|issue=1|pages=76–82|doi=10.1016/j.cub.2012.11.034|pmid=23246409}}</ref> 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.<ref>{{cite journal|last1=Walker|first1=T. N.|last2=Hughes|first2=W. O. H.|title=Adaptive social immunity in leaf-cutting ants|journal=Biology Letters|date=1 May 2009|volume=5|issue=4|pages=446–448|doi=10.1098/rsbl.2009.0107|pmc=2781909}}</ref><ref name="Royal Society B 2010">{{cite journal|last1=Ugelvig|first1=L. V.|last2=Kronauer|first2=D. J. C.|last3=Schrempf|first3=A.|last4=Heinze|first4=J.|last5=Cremer|first5=S.|title=Rapid anti-pathogen response in ant societies relies on high genetic diversity|journal=Proceedings of the Royal Society B: Biological Sciences|date=5 May 2010|volume=277|issue=1695|pages=2821–2828|doi=10.1098/rspb.2010.0644|pmid=20444720|pmc=2981995}}</ref><ref>{{cite journal|last1=Okuno|first1=Masaki|last2=Tsuji|first2=Kazuki|last3=Sato|first3=Hiroki|last4=Fujisaki|first4=Kenji|title=Plasticity of grooming behavior against entomopathogenic fungus Metarhizium anisopliae in the ant Lasius japonicus|journal=Journal of Ethology|date=15 June 2011|volume=30|issue=1|pages=23–27|doi=10.1007/s10164-011-0285-x}}</ref><ref>{{cite journal|last1=REBER|first1=A.|last2=PURCELL|first2=J.|last3=BUECHEL|first3=S. D.|last4=BURI|first4=P.|last5=CHAPUISAT|first5=M.|title=The expression and impact of antifungal grooming in ants|journal=Journal of Evolutionary Biology|date=May 2011|volume=24|issue=5|pages=954–964|doi=10.1111/j.1420-9101.2011.02230.x|pmid=21306465}}</ref>

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.<ref name=tragust /> 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.<ref name= "tragust"/> 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.<ref name="Rebeca B 2014">{{cite journal|last1=Rosengaus|first1=Rebeca B.|last2=Schultheis|first2=Kelley F.|last3=Yalonetskaya|first3=Alla|last4=Bulmer|first4=Mark S.|last5=DuComb|first5=William S.|last6=Benson|first6=Ryan W.|last7=Thottam|first7=John P.|last8=Godoy-Carter|first8=Veronica|title=Symbiont-derived β-1,3-glucanases in a social insect: mutualism beyond nutrition|journal=Frontiers in Microbiology|date=21 November 2014|volume=5|doi=10.3389/fmicb.2014.00607}}</ref>

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.<ref name="ReferenceA"/><ref name=tragust /><ref>{{cite journal|last1=Graystock|first1=Peter|last2=Hughes|first2=William O. H.|title=Disease resistance in a weaver ant, Polyrhachis dives, and the role of antibiotic-producing glands|journal=Behavioral Ecology and Sociobiology|date=24 August 2011|volume=65|issue=12|pages=2319–2327|doi=10.1007/s00265-011-1242-y}}</ref> In ants, the application of antimicrobials is often performed in conjunction with grooming, to provide simultaneous mechanical removal and chemical treatment of pathogens.<ref name=tragust /><ref>{{cite journal|last1=Yek|first1=S. H.|last2=Nash|first2=D. R.|last3=Jensen|first3=A. B.|last4=Boomsma|first4=J. J.|title=Regulation and specificity of antifungal metapleural gland secretion in leaf-cutting ants|journal=Proceedings of the Royal Society B: Biological Sciences|date=22 August 2012|volume=279|issue=1745|pages=4215–4222|doi=10.1098/rspb.2012.1458|pmid=22915672|pmc=3441083}}</ref> In ants, poison can be taken up into the mouth from the acidopore (the exit of the poison producing gland at the tip of the abdomen), and stored in the mouth, to be redistributed whilst grooming.<ref name=tragust /> In the ant ''Lasius neglectus'', the poison produced by the [[acidopore]] is composed largely of [[formic acid]] (60%), but also contains [[acetic acid]] (2%). Inhibition assays of the poison droplet against the fungal pathogen ''[[Metarhizium]]'' found that the formic acid alone substantially reduces fungal conidia viability, but that all poison components work [[synergistically]] to inhibit conidia viability, by as much as 96%.<ref name=tragust />

===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.<ref name="Royal Society B 2002"/><ref name="ReferenceC">{{cite journal|last1=Spivak|first1=Marla|last2=Reuter|first2=Gary S.|title=Resistance to American foulbrood disease by honey bee colonies bred for hygienic behavior|journal=Apidologie|date=November 2001|volume=32|issue=6|pages=555–565|doi=10.1051/apido:2001103}}</ref><ref>{{cite journal|last1=Loreto|first1=Raquel G.|last2=Hughes|first2=David P.|title=Disease in the Society: Infectious Cadavers Result in Collapse of Ant Sub-Colonies|journal=PLOS ONE|date=16 August 2016|volume=11|issue=8|pages=e0160820|doi=10.1371/journal.pone.0160820|url=http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0160820|issn=1932-6203|pmid=27529548|pmc=4986943}}</ref> As mentioned above, dead nestmates are typically removed from the nest to reduce the potential risk of disease transmission.<ref name="ReferenceB"/> Infected or not, ants that are close to death can also voluntarily remove themselves from the colony to limit this risk.<ref>{{cite journal|last1=Heinze|first1=Jürgen|last2=Walter|first2=Bartosz|title=Moribund Ants Leave Their Nests to Die in Social Isolation|journal=Current Biology|date=February 2010|volume=20|issue=3|pages=249–252|doi=10.1016/j.cub.2009.12.031|pmid=20116243}}</ref><ref>{{cite journal|last1=BOS|first1=N.|last2=LEFÈVRE|first2=T.|last3=JENSEN|first3=A. B.|last4=D’ETTORRE|first4=P.|title=Sick ants become unsociable|journal=Journal of Evolutionary Biology|date=February 2012|volume=25|issue=2|pages=342–351|doi=10.1111/j.1420-9101.2011.02425.x|pmid=22122288}}</ref> Honeybees can actively drag infected nest mates out of the hive <ref>{{cite journal|last1=Baracchi|first1=David|last2=Fadda|first2=Antonio|last3=Turillazzi|first3=Stefano|title=Evidence for antiseptic behaviour towards sick adult bees in honey bee colonies|journal=Journal of Insect Physiology|date=December 2012|volume=58|issue=12|pages=1589–1596|doi=10.1016/j.jinsphys.2012.09.014}}</ref> and may bar them from entering at all.<ref>{{cite journal|last1=Waddington|first1=Keith D.|last2=Rothenbuhler|first2=Walter C.|title=Behaviour Associated with Hairless-Black Syndrome of Adult Honeybees|journal=Journal of Apicultural Research|date=24 March 2015|volume=15|issue=1|pages=35–41|doi=10.1080/00218839.1976.11099831}}</ref> "Hygienic behaviour" is the specific removal of infected brood from the colony and has been reported in both honeybees and ants.<ref name="Royal Society B 2010"/><ref>{{cite journal|last1=Woodrow|first1=A. W.|last2=Holst|first2=E. C.|title=The Mechanism of Colony Resistance to American Foulbrood|journal=Journal of Economic Entomology|date=1 June 1942|volume=35|issue=3|pages=327–330|doi=10.1093/jee/35.3.327|url=http://jee.oxfordjournals.org/content/35/3/327|language=en|issn=0022-0493}}</ref> 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.<ref name="ReferenceC"/> Cannibalism of infected nesmtates is an effective behaviour in termites, as ingested infectious material is destroyed by antimicrobial enzymes present in their guts.<ref name="ReferenceA"/><ref name="Rebeca B 2014"/><ref>{{cite journal|last1=Rosengaus|first1=Rebeca B.|last2=Traniello|first2=James F. A.|title=Disease Susceptibility and the Adaptive Nature of Colony Demography in the Dampwood Termite Zootermopsis angusticollis|journal=Behavioral Ecology and Sociobiology|date=1 January 2001|volume=50|issue=6|pages=546–556|jstor=4602004|doi=10.1007/s002650100394}}</ref> 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.<ref name="Rebeca B 2014"/> 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.<ref name="ReferenceA"/> Some fungal pathogens (e.g. ''[[Ophiocordyceps]]'', ''[[Pandora (fungus)|Pandora]]'') manipulate their ant hosts into leaving the nest and climbing plant stems surrounding the colony.<ref>{{cite journal|last1=Hughes|first1=D. P.|last2=Araújo|first2=J. P. M.|last3=Loreto|first3=R. G.|last4=Quevillon|first4=L.|last5=de Bekker|first5=C.|last6=Evans|first6=H. C.|title=Chapter Eleven - From So Simple a Beginning: The Evolution of Behavioral Manipulation by Fungi|journal=Advances in Genetics|date=1 January 2016|volume=94|pages=437–469|url=http://www.sciencedirect.com/science/article/pii/S0065266016300049|publisher=Academic Press|doi=10.1016/bs.adgen.2016.01.004}}</ref> There, attached to the stem, they die and rain down new spores onto healthy foragers.<ref>{{cite journal|last1=Loreto|first1=Raquel G.|last2=Elliot|first2=Simon L.|last3=Freitas|first3=Mayara L. R.|last4=Pereira|first4=Thairine M.|last5=Hughes|first5=David P.|last6=Chaline|first6=Nicolas|title=Long-Term Disease Dynamics for a Specialized Parasite of Ant Societies: A Field Study|journal=PLoS ONE|date=18 August 2014|volume=9|issue=8|pages=e103516|doi=10.1371/journal.pone.0103516|pmid=25133749|pmc=4136743}}</ref> To combat these fungi, healthy ants actively search for corpses on plant stems and attempt to remove them before they can release their spores<ref>{{cite journal|last1=Marikovsky|first1=P. I.|title=On some features of behavior of the antsFormica rufa L. infected with fungous disease|journal=Insectes Sociaux|date=June 1962|volume=9|issue=2|pages=173–179|doi=10.1007/BF02224263}}</ref>

===Colony-level immunisation===

[[Immunisation]] is a reduced [[Susceptible individual|susceptibility]] to a parasite upon secondary exposure to the same parasite. The past decade has revealed that immunisation occurs in [[invertebrates]] and is active against a wide rage of parasites. It occurs in two forms: (i) specific immune priming particular parasite or (ii) a general immune up-regulation that promotes unspecific protection against a broad range of parasites. In any case, the underlying mechanisms of immunisation in invertebrates are still mostly elusive. In social animals, immunisation is not restricted to the level of the individual, but can also occur at the society level, via 'social immunisation'.<ref name=masri /> Social immunisation occurs when some proportion of the group's members are exposed to a parasite, which then leads to the protection of the whole group, upon secondary contact to the same parasite. Social immunisation has been so far described in a [[dampwood termite]]-fungus system,<ref>{{cite journal|last1=Traniello|first1=J. F. A.|last2=Rosengaus|first2=R. B.|last3=Savoie|first3=K.|title=The development of immunity in a social insect: Evidence for the group facilitation of disease resistance|journal=Proceedings of the National Academy of Sciences|date=14 May 2002|volume=99|issue=10|pages=6838–6842|doi=10.1073/pnas.102176599|pmid=12011442|pmc=124490}}</ref> a [[Lasius neglectus|garden ant]]-fungus system<ref>{{cite journal|last1=Ugelvig|first1=Line V.|last2=Cremer|first2=Sylvia|title=Social Prophylaxis: Group Interaction Promotes Collective Immunity in Ant Colonies|journal=Current Biology|date=November 2007|volume=17|issue=22|pages=1967–1971|doi=10.1016/j.cub.2007.10.029|pmid=17980590}}</ref><ref name = "konrad">{{cite journal|last1=Konrad|first1=Matthias|last2=Vyleta|first2=Meghan L.|last3=Theis|first3=Fabian J.|last4=Stock|first4=Miriam|last5=Tragust|first5=Simon|last6=Klatt|first6=Martina|last7=Drescher|first7=Verena|last8=Marr|first8=Carsten|last9=Ugelvig|first9=Line V.|last10=Cremer|first10=Sylvia|title=Social Transfer of Pathogenic Fungus Promotes Active Immunisation in Ant Colonies|journal=PLoS Biology|date=3 April 2012|volume=10|issue=4|pages=e1001300|doi=10.1371/journal.pbio.1001300|pmid=22509134|pmc=3317912}}</ref> and a [[carpenter ant]]–bacterium system.<ref>{{cite journal|last1=Hamilton|first1=C.|last2=Lejeune|first2=B. T.|last3=Rosengaus|first3=R. B.|title=Trophallaxis and prophylaxis: social immunity in the carpenter ant Camponotus pennsylvanicus|journal=Biology Letters|date=30 June 2010|volume=7|issue=1|pages=89–92|doi=10.1098/rsbl.2010.0466|pmid=20591850|pmc=3030872}}</ref> 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 <ref name="konrad"/> and termite-fungus <ref>{{cite journal|last1=Liu|first1=Long|last2=Li|first2=Ganghua|last3=Sun|first3=Pengdong|last4=Lei|first4=Chaoliang|last5=Huang|first5=Qiuying|title=Experimental verification and molecular basis of active immunization against fungal pathogens in termites|journal=Scientific Reports|date=13 October 2015|volume=5|pages=15106|doi=10.1038/srep15106|pmid=26458743|pmc=4602225}}</ref> 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]] <ref name = "konrad" />

===Organisational defence===
[[File:Interactions_in_ant_nests.png|thumb|right|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.<ref name=babz /> As disease transmission occurs through social interactions, changes in the type and frequency of these interactions are expected to modulate disease spread.<ref>{{Cite journal|last=Schmid-Hempel|first=Paul|last2=Schmid-Hempel|first2=Regula|date=1993-01-01|title=Transmission of a Pathogen in Bombus terrestris, with a Note on Division of Labour in Social Insects|jstor=4600887|journal=Behavioral Ecology and Sociobiology|volume=33|issue=5|pages=319–327|doi=10.1007/bf00172930}}</ref> Organisational immunity is predicted to have both a constitutive and an induced component. The innate, organisational substructure of social insect colonies may provide constitutional protection of the most valuable colony members, the queens and brood, as disease will be contained within subgroups. Social insect colonies are segregated into worker groups that experience different disease hazards, where the young and reproductive individuals interact minimally with the workers performing the tasks with higher disease risk (e.g. foragers).<ref name=cremer /><ref>{{cite journal|last1=Schmid-Hempel|first1=Paul|last2=Schmid-Hempel|first2=Regula|title=Transmission of a pathogen in Bombus terrestris, with a note on division of labour in social insects|journal=Behavioral Ecology and Sociobiology|date=November 1993|volume=33|issue=5|doi=10.1007/BF00172930}}</ref> This segregation can arise as a result of the physical properties of the nest<ref>{{cite journal|last1=Pie|first1=Marcio R.|last2=Rosengaus|first2=Rebeca B.|last3=Traniello|first3=James F.A.|title=Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects|journal=Journal of Theoretical Biology|date=January 2004|volume=226|issue=1|pages=45–51|doi=10.1016/j.jtbi.2003.08.002}}</ref> or the differences in space usage of the individuals.<ref>{{cite journal|last1=Mersch|first1=D. P.|last2=Crespi|first2=A.|last3=Keller|first3=L.|title=Tracking Individuals Shows Spatial Fidelity Is a Key Regulator of Ant Social Organization|journal=Science|date=18 April 2013|volume=340|issue=6136|pages=1090–1093|doi=10.1126/science.1234316|pmid=23599264}}</ref> It can also result from age- or task-biased interactions.<ref>{{cite journal|last1=Scholl|first1=Jacob|last2=Naug|first2=Dhruba|title=Olfactory discrimination of age-specific hydrocarbons generates behavioral segregation in a honeybee colony|journal=Behavioral Ecology and Sociobiology|date=9 June 2011|volume=65|issue=10|pages=1967–1973|doi=10.1007/s00265-011-1206-2}}</ref> Distinct activity patterns between group members (e.g. individuals with relatively higher number of interactions, or high number of interaction partners) has also been hypothesized to influence disease spread.<ref>{{cite journal|last1=Naug|first1=Dhruba|last2=Camazine|first2=Scott|title=The Role of Colony Organization on Pathogen Transmission in Social Insects|journal=Journal of Theoretical Biology|date=April 2002|volume=215|issue=4|pages=427–439|doi=10.1006/jtbi.2001.2524}}</ref> It is further assumed that social insects may further modulate their [[interaction network]]s upon disease coming into the colony. However, the organisational immunity hypothesis is currently mainly supported by theoretical models and awaits empirical testing.<ref name="babz" />

==References==
{{reflist}}

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[[Category:Immunology]]

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