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Social immunity and the evolution of group living in insects rstb.royalsocietypublishing.org Joe¨l Meunier Zoological Institute, Evolutionary Biology, Johannes Gutenberg University Mainz, Mainz, Germany

Review Cite this article: Meunier J. 2015 Social immunity and the evolution of group living in insects. Phil. Trans. R. Soc. B 370: 20140102. http://dx.doi.org/10.1098/rstb.2014.0102 Accepted: 2 December 2014 One contribution of 14 to a theme issue ‘The sociality– health – fitness nexus in animal societies’. Subject Areas: behaviour, evolution Keywords: personal immunity, behavioural immunity, collective immunity, parasite, social evolution, insects Author for correspondence: Joe¨l Meunier e-mail: [email protected]

Electronic supplementary material is available at http://dx.doi.org/10.1098/rstb.2014.0102 or via http://rstb.royalsocietypublishing.org.

The evolution of group living requires that individuals limit the inherent risks of parasite infection. To this end, group living insects have developed a unique capability of mounting collective anti-parasite defences, such as allogrooming and corpse removal from the nest. Over the last 20 years, this phenomenon (called social immunity) was mostly studied in eusocial insects, with results emphasizing its importance in derived social systems. However, the role of social immunity in the early evolution of group living remains unclear. Here, I investigate this topic by first presenting the definitions of social immunity and discussing their applications across social systems. I then provide an up-to-date appraisal of the collective and individual mechanisms of social immunity described in eusocial insects and show that they have counterparts in non-eusocial species and even solitary species. Finally, I review evidence demonstrating that the increased risks of parasite infection in group living species may both decrease and increase the level of personal immunity, and discuss how the expression of social immunity could drive these opposite effects. By highlighting similarities and differences of social immunity across social systems, this review emphasizes the potential importance of this phenomenon in the early evolution of the multiple forms of group living in insects.

1. Introduction The shift from a solitary life to group living is considered to be one of the major evolutionary transitions [1,2]. To date, group living can be found in almost all animal taxa, with its complexity ranging from simple mutual attraction between individuals, over temporary periods of parental care in family associations, to permanent societies with reproductive division of labour [3,4]. The ecological success of group living species is traditionally thought to rely on the fitness benefits social life provides to group members, such as improved protection against predators, increased reproductive success, enhanced foraging efficiency and higher survival rates [5]. However, group living also comes with major fitness costs. One of these costs is the increased risks of parasite infection (broadly defined to include bacteria, viruses, protozoans, helminths and fungi) [6– 12]. These risks are particularly exacerbated in group living species, because frequent and intimate contacts between individuals are known to facilitate parasite transmission, and because the close genetic relatedness often exhibited by group members is likely to make them susceptible to the same parasites [6,7,13 –15]. Hence, to gain a better understanding of the evolution of group living, we need to shed light on the mechanisms that limit the inherent risks of parasite infections for group living individuals [7]. Group living individuals are not only able to limit parasite infection using their personal immune system [16,17], but may also use their unique capability of mounting collective defences. This phenomenon, called social immunity (see below for a more detailed definition [6,7,18]), encompasses multiple mechanisms such as the use of antimicrobial substances as nest material and sanitation behaviours to eliminate corpses and waste products from the nest (figure 1). Over the last 20 years, eusocial insects, which mostly include ants, termites, as well as some bees and wasps, have provided one of the main biological models to study social immunity [7,19–21]. The resulting studies were of key importance, because they revealed the structural diversity of social immunity across eusocial species and

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(f)

(d )

(g)

Figure 1. Examples of social immunity in insects. (a) A female of the European earwig Forficula auricularia cleaning her eggs from fungal spores (Picture credit: J. Meunier). (b) Workers of the invasive garden ant Lasius neglectus allogrooming a colour-marked nest-mate exposed to an entomopathogenic fungus (Picture credit: M. Konrad, IST Austria). (c) In the dampwood termite Zootermopsis angusticollis, workers express alarm behaviours to limit the spread of pathogens among colony members (Picture credit: R. Rosengaus). (d) A worker of the wood ant Formica paralugrubris using resin as nest material to enhance protection against parasite infections (Picture credit: A. Maeder). (e) A worker of the ant Camponotus sp. carrying a corpse away from the nest (Picture credit: L. Diez). (f ) Honeybee workers removing diseased larvae from an uncapped cell (Picture credit: G. Bigio). (g) A female of the burying beetle Nicrophorus vespilloides using the antimicrobial properties of her anal exudates to protect the nest against parasites (Picture credit: O. Krueger). (Online version in colour.)

provided clear evidence for the importance of this phenomenon in permanent and complex social groups [7,19]. However, these studies were of limited relevance for our understanding of the role of social immunity in the early evolution of social life. In particular, it remains unclear whether social immunity only emerged in eusocial systems and therefore represents a secondary trait derived from eusociality, or whether it has counterparts in less derived forms of group living and thus possibly plays a role in the emergence and maintenance of group living. The aim of this review is to explore whether social immunity is a driver or a by-product of the evolution of complex forms of group living in insects. This review focuses on insects, because they exhibit the greatest diversity of social systems across animal taxa [3,4], including most of the eusocial species currently known, and because they represent a majority of the studies in which social immunity has been studied [7,15,22]. I begin by presenting different definitions of social immunity found in the literature and discuss their importance to study this phenomenon across social systems. I then provide an upto-date appraisal of the collective and individual anti-parasite mechanisms reported in eusocial insects and, where applicable, link these mechanisms to their known counterparts in noneusocial and solitary species [23]. Non-eusocial species are defined as all species in which group living is temporary or permanent, facultative or obligatory, but where it is not associated with reproductive division of labour (for a full description of the multiple forms of group living, see [3,4]). In a third part, I review empirical evidence showing the positive and negative influence of group living on the expression of personal immunity and discuss the role of social immunity on the nature of these effects. Finally, I discuss how currently available data provide insights on the possible role of social immunity in the evolution of group living, but also emphasize the need to study social immunity in a larger number of non-eusocial insects.

2. Definitions of social immunity The first definition of social immunity in an evolutionary context was offered in a landmark paper published in 2007 by

Cremer et al. [7]. They defined social immunity as ‘collective action or altruistic behaviours resulting in avoidance, control or elimination of parasitic infections’. This definition, followed by the shorter one ‘collective defences against parasites and pathogens’ by Wilson-Rich et al. in 2009 [19], was coined to describe the group-level defences against parasites expressed in colonies of eusocial insects (and to some extent in groups of primates). These defences included allogrooming, a behaviour during which one individual grooms another individual to remove its external parasites, and hygienic behaviours, during which diseased brood are removed from the nest [7,19] (see also figure 1). In an important review published in 2010, Cotter & Kilner [23] proposed to broaden the field of social immunity by applying the theory previously developed in the context of eusocial insects to other forms of group living. To this end, social immunity was defined as ‘any type of immune response that has been selected to increase the fitness of the challenged individual and one or more recipients’. One major benefit of defining social immunity in a broader context than eusociality was to allow the inclusion of anti-parasite defences that are not tightly linked to permanent social organization, such as parental care during family life (e.g. [24]) and to some extent herd immunity [25] (see also conclusion in [7]). Another benefit of the definition by Cotter et al. was that it clarified that social immunity refers to defences that have been selected for their collective anti-parasite protection, and not the ones that provide benefits to group members as a simple by-product of personal protection. This distinction is of key importance, because social immunity could otherwise encompass the strategies used by solitary-living individuals to fight their own infection, as these strategies somewhat reduce parasite exposure of the conspecifics they might encounter during their life cycle (e.g. during mating or competitive interactions). The definition proposed by Cotter & Kilner [23] also raised two potential issues. First, it frees the recipients from being a member of the donors’ group, so that social immunity might not be a product of social life, but simply the outcome of shared location between individuals (even from different species) [23]. For instance, this definition allowed social

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Infecting multiple members of an insect group generally requires that parasites successively pass three steps [7,19]. The first one consists of the uptake of the parasite from the environment, the second step is its successful transfer into the nest and the third one is its multiplication and transmission to other group members. Any individual or collective strategy reducing the success of parasites in at least one of these three steps thus possibly qualifies as a mediator of social immunity (given that its collective benefits are under selection). In their seminal study, Cremer et al. [7] reviewed the large diversity of anti-parasite mechanisms employed by eusocial insects to diminish the risks associated with each of the three steps of infection. Some of these mechanisms require traits that are specific to eusocial systems, such as division of labour, so that their expression is unlikely to exist in other forms of group living. However, many of them do not have such requirements, which offers scope for their expression in noneusocial species, and even to find counterparts in solitary species [23]. In the following sections, I provide an up-to-date appraisal of the anti-parasite mechanisms involved in each of the three steps of group infection in eusocial insects (adapted from Cremer et al. [7]) and then determine whether they have known counterparts in non-eusocial and solitary insects. I summarize what is known in table 1, which is organized around the three steps to infection just described. Based on this information, I then discuss potential reasons for the presence/absence of these defences across the different forms of group living.

(a) Step 1: limiting parasite uptake from the environment The most common strategies used by eusocial insects to limit parasite uptake from the environment encompass both collective and individual mechanisms that help to avoid infection after or during foraging activities. Collective defences are illustrated, for instance, by guards of the honeybee Apis mellifera, which prevent newly infected nest-mates from entering the hive [38] and ‘hitchhikers’ of leaf-cutter ants, which ride on leaf fragments to defend foragers against parasitoid attacks

(b) Step 2: limiting parasite establishment into the nesting habitat Incorporating chemical/antimicrobial substances into the nest material and/or expressing nest sanitation behaviours are the two main processes reported in eusocial insects to prevent parasite establishment in their habitat. Chemical substances can be collected from the environment, such as in the wood ant Formica paralugubris and the honeybee in which workers collect pieces of resin and incorporate them into nest structure (figure 1, [39,40]), or they may be synthesized by colony members through metapleural, sternal or venom glands [41 –43,83] (reviewed in [84]). Sanitation behaviours involve eliminating waste material, such as conspecific corpses, left-over food or frass that could be used as a substrate by the parasites [54,55,85]. The use of chemical/antimicrobial substances and sanitation behaviours can also be found in many non-eusocial species [84]. For instance, adults of the group living beetle Dendroctonus rufipennis exude oral secretions in their galleries to inhibit the growth of colonizing fungi [44]. Subsocial females of the beewolf Philanthus triangulum cultivate Streptomyces bacteria on their antenna and apply them to brood cells to protect cocoons from fungal infection [45]. Frass removal occurs in the subsocial cockroach Cryptocercus punctulatus [57], the group living beetle Trachyostus ghanaensis [58] and the subsocial cricket Anurogryllus muticus [59]. Frass removal can even be found in solitary insects exhibiting high site fidelity, such as the grasshopper Atractomorpha lata and in Epargyreus clarus caterpillars, in which frass pellets are ballistically ejected by the producing individuals [56,60]. Interestingly, an alternative strategy to frass removal is to imbue frass or anal exudates with antimicrobial properties and use them in the nest to limit parasite establishment. This process occurs in both eusocial (termites) and non-eusocial (cockroaches and burying beetles) species, in which the use

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3. Social immunity in eusocial, non-eusocial and solitary insects

[37]. On the other hand, individual defences can be exhibited by foragers that avoid habitats containing entomopathogenic fungi and nematodes, such as in the termite Macrotermes michaelseni and the ant Solenopsis invicta [27,28], respectively, as well as by other ant species that refrain from the consumption of contaminated food or conspecifics [32,33]. The individual anti-parasite mechanisms reflected by avoidance behaviours are not specific to eusocial insects and can be found in many non-eusocial and solitary species. For example, gregarious individuals of the migratory grasshopper Melanoplus sanguinipes and the German cockroach Blattella germanica avoid the consumption of contaminated food/conspecifics [34,35]. In the subsocial burying beetle Nicrophorus vespilloides, females avoid degraded carcasses (covered with many microbes) if given a choice with fresh ones, a mechanism that could also have evolved to reduce post-hatching competition between juveniles and microbes over the carcass [30]. Finally, in the solitary-living Japanese beetle Popillia japonica and the seven-spot ladybird Coccinella septempunctata, individuals avoid soil contaminated with entomopathogenic fungi [31] and larvae inhibit their consumption of infected prey [36], respectively. Because avoidance behaviours provide direct fitness benefits to the actors, the importance of social interactions in the emergence and/or persistence of these behaviours in social species, and thus their qualification as social immunity, remains to be further explored [7].

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immunity to encompass symbionts protecting their hosts, which is unlikely to reflect social life. The second potential issue comes from the strong emphasis on the fitness benefits for both donor and recipient(s). This may suggest that no cost is involved in social immunity, which in addition to being an unlikely scenario (e.g. [26]), would also raise the question of why not all anti-parasitic defences have evolved towards this universally beneficial state. To circumvent the issues raised by the definition of Cotter & Kilner [23] while adopting their proposal to expand the field of social immunity beyond eusociality, I propose to define social immunity as ‘any collective and personal mechanism that has emerged and/or is maintained at least partly due to the antiparasite defence it provides to other group members’. Readers interested in details of terminologies covering individual and social immunization are referred to the review by Masri & Cremer [22].

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requirements

eusocial

non-eusocial (group living)

solitary

Step 1. Limiting parasite uptake from the environment only a small proportion of group members forage

stable habitat (e.g. nest)

[113]

x

x

[27 – 29,114 –

[30,117]

[31,118 – 120]

[32,33,121 – 124]

[34,35]

[36,119,120, 125– 127]

[37]

x

x

[38,128]

x

x

[39,40,129, 130]

?

x

stable habitat (e.g. nest)

[20,41 –43,131 – 134]

[44,45,135]

x

faecal material/anal exudates with antimicrobial properties cover the nest

stable habitat (e.g. nest)

[46 – 48]

[26,49 – 53, 136,137]a

x

corpse removal garbage and frass removal/separated waste dump

stable habitat (e.g. nest) stable habitat (e.g. nest)

[54,138 – 144] [55,56,145 – 150]

? [56 – 59,

x [60]b [56]

cover/encapsulate corpses or parasites within the nest

stable habitat (e.g. nest)

[33,143,155 –

?

x

division of labour avoidance of contaminated habitats (incl. oviposition places)

116]

avoidance of consumption/contact with infected food/ conspecifics (incl. cannibalism) guarding of foraging trails

guarding of nest entrance

stable habitat (e.g. nest) foraging trails division of labour stable habitat (e.g. nest) division of labor

Step 2. Limiting parasite establishment into the nesting habitat collection of antimicrobial substances stable habitat (e.g. nest) use of self-produced chemical secretions on habitat surface (e.g. metapleural or sternal glands, venom, other)

151 – 154] 157] Step 3. Limiting parasite transmission between group members (a) From adults to brood mechanical removal by allogrooming (adults-to-brood) application of antimicrobial secretion on the brood/

parental/sibling care parental/sibling care

[20,158] [61,161 – 163]

[24,159,160] [24]c

x x

feed the brood with anti-parasitic components infected individuals do not tend the queen/brood

parental/sibling care communal breeding or

[62,164 – 166] [64,65]

[63,167 – 172] ?

x x

removal of diseased brood

precocial species parental/sibling care

[66,67,173,174]

?

x

[68,175]

[69]

[176– 180]d

[20,33,64,70,71,

[72]e

x

158,181 –192] [73,193]

[74]f

[74]f

[13,113, 194– 198]

?

x

[65,75,199,200]

?

x

the eggs

trans-generational immune priming (b) From adults to adults mechanical removal by allogrooming (adult-to-adult)

behavioural interactions

social fever spatial compartmentalization of the nest/digging area

stable habitat (e.g. nest) complex nest architecture

infected individuals leave the group/limit contact to group members

(Continued.)

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defence mechanisms

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Table 1. Personal and collective mechanisms shaping social immunity in eusocial insects, and their counterparts in non-eusocial and solitary species. Requirements for their expression are listed for each mechanism. The mechanisms can be absent/not reported (?) or not expected to occur in the given system (x). Table adapted from Cremer et al. [7], which also contains information on whether these defences are prophylactic or induced. References [113– 219] are given in the electronic supplementary material.

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Table 1. (Continued.)

eusocial

behavioural structuring (castes/age)

overlapping generations or castes

[6,201,202]

x

x

indirect interaction with garbage workers

stable habitat (e.g. nest) division of labour

[145]

x

x

defence mechanisms

pathogen alarm

[71,76]

?

x

[29]

?

x

[66,67,77,158, 174,203 –207]

?

x

stable habitat (e.g. nest)

[20,78,124]

?

x

behavioural interactions

[65,70,208]

?

x

stable group composition

[66,79,80, 209– 216]

but see [81]

x

[82,217,218]

?

x

stable habitat (e.g. nest) complex nest

remove/cannibalize infected individuals/brood from the group abandon infected nests immunity transfer by social interactions (c) Genetic adaptations increased genetic diversity (multiple mating, multiple queens) increased recombination rates a

In burying beetles, this mechanism could help mothers and offspring to limit competition with microbes over the carcasses. Frass ejection. c Application of cuticular hydrocarbons on the brood. d Could also be considered as a form of parental care [219]. e Role against parasite infection still unclear. f Behavioural fever. b

of frass as nest material has been shown to limit parasite development [46,47,49–51]. The maintenance of frass in the nest may also provide immune benefits by allowing exchanges of endosymbionts and other immune factors among group members. For instance, in the bumblebee Bombus terretris, individuals obtain bacterial microbiota by feeding on conspecific faeces, which improves their resistance against the protozoan parasite Crithidia bombi [48]. To date, this latter benefit remains unexplored in non-eusocial insects.

(c) Step 3: limiting parasite transmission between group members When a parasite has successfully passed the two first steps of group infection, the expression of mechanisms limiting its transmission among group members is required. Eusocial and non-eusocial species share most of the mechanisms known to limit the transmission of parasites from adults to offspring (including eggs and juveniles). This is expected as many group living species with non-eusocial systems are characterized by various forms of parental care, which possibly include anti-parasite defences [86]. These mechanisms include adults grooming the brood to remove external parasites [20,24], applying antimicrobial secretions to the brood [24,61], providing food with antimicrobial properties to the brood [62,63] or transferring immune components to their eggs (called trans-generational immune priming [68,69]). The mechanisms solely present in eusocial insects consist of workers eliminating infected brood (hygienic behaviour, [66,67]) or of infected individuals avoiding contact with the

brood [64,65]. Nevertheless, these two mechanisms could be expected in subsocial (and precocial) species. Limiting parasite spread between group members is not only important for the brood, but also for adults. In eusocial species, multiple processes are known to limit parasite spread among adults, such as building nest architecture with small chamber areas [13], abandoning infected nests [78], boosting personal immunity by social contacts [70] or consuming infected group members [77] (table 1). Individuals of the dampwood termite Zootermopsiss angusticollis also express pathogen alarm behaviours when encountering infected conspecifics [71] (but also infected environments [76]), a behaviour that prevents pathogen spread among individuals by triggering avoidance behaviours. Infected individuals may also be isolated from the group either through exclusion, such as in the subterranean termite Reticulitermes tibialis [29], or through self-driven desertion (due to their moribund state), as in the ant Temnothorax unifasciatus [75]. Although the above processes do not necessarily require traits that are specific to eusocial insects (table 1), only allogrooming has been found in non-eusocial and/or solitary species. This behaviour is ubiquitous in eusocial insects [87], in which it reduces the presence of external parasites on the receiving individual, as well as improving the immune response of the donor through low dose infection [70]. Allogrooming has also been reported in non-eusocial insects, such as earwigs and cockroaches [72,88], but its importance in reducing parasite infection remains unclear. Note that the mediator of social fever is also not specific to eusocial systems. Social fever is a collective defence during which group members adaptively and temporarily increase their

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isolation of infected individuals

solitary

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requirements

non-eusocial (group living)

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Although several mechanisms of social immunity are common to eusocial and non-eusocial species, others are unexpectedly absent in non-eusocial insects living in nests (e.g. during family life). This is the case, for instance, for corpse removal from the nest, abandoning of infected nests, increase in group genetic diversity to prophylactically resist against parasite infection, isolation of infected individuals or group desertion by infected individuals (table 1). One potential explanation for this lack of evidence is the very limited number of studies investigating social immunity in non-eusocial insects, even if a growing number of studies recently have started to fill this gap (e.g. [24,52,53]). Another possible explanation is that the emergence of these mechanisms depends on traits that are specific to eusocial insects, but not directly associated with their social system. For instance, colonies of eusocial insects are mostly composed of non-reproductive individuals, for which social immunity is the only way to protect the queen’s brood and thus to favour their own (indirect) fitness under parasite attack [19]. Similarly, eusocial colonies may contain a large number of individuals, which could increase the efficiency and thus the use of collective anti-parasite defences compared with smaller groups [19]. Further research should thus be conducted to (i) enlarge the number of studies testing the expression of social immunity in non-eusocial species and to (ii) determine the importance of eusocial-derived traits on the emergence and expression of these collective defences. Even if many studies reveal the occurrence of social immunity in eusocial species, it is important to note that others have failed at providing relevant support. For instance, queens of the wood ant F. paralugubris are specifically attracted to (instead of repelled from) habitats contaminated by entomopathogenic fungi [92]. Similarly in the pharaoh ant Monomorium pharaonis, colonies preferentially move into infected nests when

4. Personal immunity and group living The early evolution of group living and its associated risks of parasite infection may not only have favoured the emergence of social immunity, but may also have selected for higher effort in personal immune responses. This higher effort would help group living individuals both to prophylactically limit a greater per capita risk of infection (density-dependent prophylaxis hypothesis, called DDP [96]) and to benefit from herd immunity, which is generated by the accumulation of resistant individuals within a group [97]. A series of three studies recently provided empirical support for DDP’s prediction of a positive association between group living and efforts in personal immunity [98 –100]. In these studies, authors compared the level of personal immunity across six species of bees, nine species of wasps and six species of thrips exhibiting a gradient of sociality ranging from solitary to eusocial. Each of these three studies showed that the antimicrobial secretions present on individuals’ cuticles were significantly more efficient in eusocial compared with solitary species. Empirical support for this prediction also comes from within-species comparisons. For instance, in the desert locust Schistocerca gregaria, individuals in the gregarious phase showed higher antimicrobial activities and survived infections better than individuals in the solitary phase [101] (see other examples in [96]). By contrast, it has been proposed that the emergence of social immunity could reduce the expression of personal immunity due to investment trade-offs between these two processes [7,23,90]. Three genomic and two physiological studies conducted with eusocial and non-eusocial insects supported this prediction. The genomic analyses showed that (i) the number of gene families implicated in immunity was three times lower in honeybees than in two solitary insects [90,102], that (ii) experimentally isolated Bombus terrestris workers up-regulated the expression of immune-related genes [103] and that (iii) the number of immunerelated genes expressed in infected S. gregaria individuals was higher when they lived in the solitary compared with gregarious phase [104]. Moreover, the physiological studies revealed that across 12 Lepidoptera species, the caterpillars feeding solitarily had higher levels of personal immunity than the ones feeding gregariously [8]. Finally, in the Australian plague locusts Chortoicetes terminifera, the level of personal immunity was negatively correlated with population densities, while experimental isolation of individuals marching in bands yielded an increase in their personal immune levels [105].

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(d) Ubiquity of collective immunity across group living insects?

presented with the choice between an infected and an uninfected one [93]. Finally, workers of the termite Z. angusticollis do not discriminate between infected and non-infected conspecifics [94], and parasite infection does not increase the expression of allogrooming in the ant Formica selysi [95]. Overall, these results provide important insights into the link between group living and social immunity because they (i) reveal that not all the mechanisms of social immunity are necessarily expressed during group living and (ii) shed light on the potential role of other factors, e.g. parasitic strategies and life-history costs, in the expression of collective defences. Furthermore, these results suggest that social immunity is not always the most efficient defence against parasite infection, which raises questions about the importance of personal immunity in group living individuals.

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own temperature (behavioural fever) to increase nest temperature (then called social fever) to a level that is detrimental for parasites. This collective defence has only been reported in honeybees [73], but behavioural fever is a common antiparasite defence in non-eusocial and solitary species (reviewed in [74]). Whether behavioural fever can be elevated to social fever in non-eusocial insects remains unknown. Finally, the increase in genetic diversity within a group is also known to help prophylactically in reducing the risk of parasite spread between group members, including both adults and juveniles [89,90]. In eusocial insects, this resistance can be achieved by increasing the number of queens and/or of the queen’s mating partners, as revealed by the higher survival rates of ant and honeybee workers living in infected colonies headed by multiple compared to single queens [79] or by multiply compared to singly mated queens [80], respectively. The benefits of increased genetic diversity have also been proposed to result from genomic recombination, which occurs at high rates in several eusocial species [82] (but see [91]). Somewhat surprisingly, the importance of group genetic diversity for parasite resistance remains poorly studied in non-eusocial insects. To the best of my knowledge, only a single study (indirectly) tested this effect in a gregarious insect, caterpillars of the moth Malacosoma californicum pluviale, but reported inconclusive results [81].

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Better understanding of whether social immunity is a driver or a by-product of the evolution of complex forms of group living first requires data on its occurrence across social systems [23]. This review reveals that out of the 30 individual and collective mechanisms known to mediate social immunity in eusocial insects and listed in table 1, 10 have counterparts in non-eusocial and four in solitary species. The distribution of these mechanisms across social systems is compatible with a scenario placing social immunity as a prerequisite for increased complexity in the nature and frequency of social interactions (i.e. in the evolution of group living). In particular, eusocial insects express the individual mechanisms used by solitary species to limit parasite uptake from the environment (first step of parasite infection), to which they add the collective ones used by non-eusocial species to limit both parasite establishment in the nest (second step of parasite infection) and parasite transmission to the brood (first part of the third step of parasite infection), as well as specific ones that limit parasite spread between adult group members (second part of the third step of parasite infection). Note, however, that this scenario does not exclude that (at least) some collective mechanisms are secondarily evolved in eusocial systems. The second step to establish an important role for social immunity in the early evolution of social life is to show that its personal and collective mechanisms are at least partly selected for their collective benefits. To date, however, this

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5. Discussion

important step lacks experimental evidence. One possible reason is that some of the mechanisms of social immunity are known to mediate other key processes in insects, so testing their immune benefits while preventing the expression of their other properties is experimentally difficult. For instance, frass removal can serve to limit parasite establishment in the nesting habitats, but also to eliminate chemical cues used by parasites to detect host presence, or simply to free space from confined areas [56]. Allogrooming not only helps individuals to remove ectoparasites, but also to share chemical compounds with other nest-mates and consequently to improve the accuracy of nest-mate recognition by homogenizing chemical signatures among group members [108]. Finally, increasing genetic diversity prophylactically limits the spread of parasites among group members, but also shapes the level of social conflicts (e.g. between queens and workers over male production [109]) and improves the efficiency of division of labour [110]. Another reason for this lack of empirical evidence is that most of the currently available data come from eusocial insects, which is not ideal to determine whether social immunity is a driver or a by-product of the evolution of group living [23]. Testing this question indeed requires researchers to disentangle the fitness of the donor individual from that of the recipient, which is experimentally difficult (if not impossible) when the vast majority of group members is sterile or never reproduces, as in eusocial insects. To circumvent this difficulty, one option is to study the benefits of collective forms of immunity in queens that found a new colony (e.g. [111]). However, the specificity of the foundation phase might not properly reflect the selection pressures shaping ancestral eusocial colony life. Another option is to study the benefits of collective forms of immunity in non-eusocial species [23], as their group members traditionally express full reproductive capabilities and thus have experimentally quantifiable individual fitness. Compared to eusocial species, the non-eusocial ones can also be used to investigate temporal trade-off between social and personal immunity, as their group members possibly experience solitary and group living phases during their life cycle. For instance, solitary phases alternate with group living phases in the migratory locust, solitary life takes turns with family life in subsocial insects such as burying beetles, and juveniles even have the capability to choose between family or solitary life in the European earwig Forficula auricularia [112]. Finally, increasing the number of studies on social immunity in non-eusocial species would permit phylogenetic studies that are balanced across taxonomic groups and social systems, and, thus, to properly trace the early evolution of collective defences in insects. In conclusion, using an up-to-date appraisal of the multiple forms of collective immunity reported in group living insects, this review highlights the fact that collective immunity is not limited to eusocial species (see also [23]). The distribution of these mechanisms across the continuum from solitary to eusocial insects suggests that social immunity is a tenet of social evolution, even if some collective mechanisms could be by-products of derived forms of group living. This review also emphasizes that the vast majority of studies on social immunity have focused on eusocial taxa, which calls for future empirical and theoretical research investigating its occurrence across a broader spectrum of group living species. Such additional studies would be particularly interesting, as they would allow conducting phylogenetic studies to reconstruct the evolutionary pathways and timing of collective defences and would more generally offer a novel framework to better

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The discrepancy between these positive and negative associations sheds light on the two main assumptions required to expect a negative effect of group living on personal immunity. The first one is that group living is associated with the expression of social immunity, which is not necessarily the case in all group living insects (see above). The second one is that mounting a collective immune response is costly for the producers. To the best of my knowledge, only one study investigated this cost in a (sub)social insect. In particular, Cotter et al. [26] showed in the burying beetle N. vespilloides that increased investment in wound repair ( personal immunity) caused a temporary decrease in the antibacterial activity of anal exudates (social immunity) of mothers. These exudates are used by the parents to limit microbial development on the carcass hosting their developing offspring [30]. This important finding raises questions about the general costs of social immunity across social systems and thus of its importance in the expression of personal immunity. Both questions call for further studies addressing this issue in a large number of eusocial and non-eusocial species. It is important to note, however, that the expression of such costs may depend on the intrinsic quality of the individuals, so that high-quality individuals could afford relatively high investment into both personal and social immune responses [106]. As a result, any variation in individual quality within a population could have the potential to prevent detection of the trade-off between the two types of immunity, or even to transform it into a false-positive association at the population (or species) level [107]. Future studies on the costs of mounting forms of collective immunity should therefore control for individual quality, e.g. by experimentally upregulating the social or personal immune response of a given individual and then looking for downregulation in other areas (e.g. [26]).

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understand the role of parasite pressures on the emergence, transformation and/or disruption of social life. tunity to contribute to this issue. I also thank S. Foitzik, P. Kappeler,

References 1.

3. 4. 5.

6. 7.

8.

9.

10.

11.

12.

13.

14.

15.

16. 17.

18. Schmid-Hempel P. 2005 Evolutionary ecology of insect immune defenses. Annu. Rev. Entomol. 50, 529 –551. (doi:10.1146/annurev.ento.50.071803. 130420) 19. Wilson-Rich N, Spivak M, Fefferman NH, Starks PT. 2009 Genetic, individual, and group facilitation of disease resistance in insect societies. Annu. Rev. Entomol. 54, 405–423. (doi:10.1146/annurev.ento. 53.103106.093301) 20. Oi DH, Pereira RM. 1993 Ant behavior and microbial pathogens. Florida Entomol. 76, 63 –74. (doi:10. 2307/3496014) 21. Evans JD, Spivak M. 2010 Socialized medicine: individual and communal disease barriers in honey bees. J. Invertebr. Pathol. 103, S62–S72. (doi:10. 1016/j.jip.2009.06.019) 22. Masri L, Cremer S. 2014 Individual and social immunisation in insects. Trends Immunol. 35, 471– 482. (doi:10.1016/j.it.2014.08.005) 23. Cotter SC, Kilner RM. 2010 Personal immunity versus social immunity. Behav. Ecol. 21, 663–668. (doi:10.1093/beheco/arq070) 24. Boos S, Meunier J, Pichon S, Ko¨lliker M. 2014 Maternal care provides antifungal protection to eggs in the European earwig. Behav. Ecol. 25, 754–761. (doi:10.1093/beheco/aru046) 25. John TJ, Samuel R. 2000 Herd immunity and herd effect: new insights and definitions. Eur. J. Epidemiol. 16, 601– 606. (doi:10.1023/ A:1007626510002) 26. Cotter SC, Topham E, Price AJP, Kilner RM. 2010 Fitness costs associated with mounting a social immune response. Ecol. Lett. 13, 1114– 1123. (doi:10.1111/j.1461-0248.2010.01500.x) 27. Drees BM, Miller RW, Vinson BS, Georgis R. 1992 Susceptibility and behavioral response of red imported fire ant (Hymenoptera: Formicidae) to selected entomogenous nematodes (Rhabditida: Steinernematidae & Heterorhabditidae). J. Econ. Entomol. 85, 365–370. (doi:10.1093/jee/85.2.365) 28. Mburu DM, Ochola L, Maniania NK, Njagi PGN, Gitonga LM, Ndung’u MW, Wanjoya AK, Hassanali A. 2009 Relationship between virulence and repellency of entomopathogenic isolates of Metarhizium anisopliae and Beauveria bassiana to the termite Macrotermes michaelseni. J. Insect Physiol. 55, 774– 780. (doi:10.1016/j.jinsphys.2009.04.015) 29. Epsky ND, Capinera JL. 1988 Efficacy of the entomogenous nematode Steinernema feltiae against a subterranean termite, Reticulitermes tibialis (Isoptera: Rhinotermitidae). J. Econ. Entomol. 81, 1313–1317. (doi:10.1093/jee/81.5.1313) 30. Rozen DE, Engelmoer DJP, Smiseth PT. 2008 Antimicrobial strategies in burying beetles breeding

31.

32.

33.

34.

35.

36.

37.

38.

39.

40.

41.

42.

on carrion. Proc. Natl Acad. Sci. USA 105, 17 890– 17 895. (doi:10.1073/pnas.0805403105) Villani MG, Krueger SR, Schroeder PC, Consolie F, Consolie NH, Preston-Wilsey LM, Donald RW. 1994 Soil application effects of Metarhizium anisopliae on Japanese Beetle (Coleoptera: Scarabaeidae) behavior and survival in turfgrass microcosms. Environ. Entomol. 23, 502–513. (doi:10.1093/ee/23.2.502) Baur ME, Kaya HK, Strong DR. 1998 Foraging ants as scavengers on entomopathogenic nematodekilled insects. Biol. Control 236, 231– 236. (doi:10. 1006/bcon.1998.0635) Kramm KR, West DF, Rockenbach PG. 1982 Termite pathogens?: transfer of the entomopathogen Metarhizium anisoploae between Reticulitermes sp. termites. J. Invertebr. Pathol. 40, 1–6. (doi:10. 1016/0022-2011(82)90029-5) Jaronski ST. 2013 Mycosis inhibits cannibalism by Melanoplus sanguinipes, M. differentialis, Schistocerca americana, and Anabrus simplex. J. Insect Sci. 13, 1–9. (doi:10.1673/031.013.12201) Kaakeh W, Reid BL, Bennett GW. 1996 Horizontal transmission of the entomopathogenic fungus Metarhizium anisopliae and hydromethylnon among German cockroaches. J. Entomol. Sci. 31, 378 –390. Roy HE, Pell JK, Clark SJ, Alderson PG. 1998 Implications of predator foraging on aphid pathogen dynamics. J. Invertebr. Pathol. 71, 236–247. (doi:10.1006/jipa.1997.4736) Vieira-Neto EHM, Mundim FM, Vasconcelos HL. 2006 Hitchhiking behaviour in leaf-cutter ants: an experimental evaluation of three hypotheses. Insectes Soc. 53, 326–332. (doi:10.1007/s00040006-0876-7) Waddington KD, Rothenbuhler WC. 1976 Behaviour associated with hairless-black syndrome of adult honeybees. J. Apic. Res. 15, 35 –41. Simone-Finstrom M, Spivak M. 2010 Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41, 295 –311. (doi:10.1051/apido/2010016) Christe P, Oppliger A, Bancala` F, Castella G, Chapuisat M. 2003 Evidence for collective medication in ants. Ecol. Lett. 6, 19 –22. (doi:10. 1046/j.1461-0248.2003.00395.x) Yek SH, Mueller UG. 2011 The metapleural gland of ants. Biol. Rev. Camb. Philos. Soc. 86, 774– 791. (doi:10.1111/j.1469-185X.2010.00170.x) Rosengaus RB, Traniello JFA, Lefebvre ML, Maxmen AB. 2004 Fungistatic activity of the sternal gland secretion of the dampwood termite Zootermopsis angusticollis. Insectes Soc. 51, 259 –264. (doi:10. 1007/s00040-004-0749-x)

Phil. Trans. R. Soc. B 370: 20140102

2.

Szathmary E, Maynard Smith J. 1995 The major evolutionary transitions. Nature 374, 227–232. (doi:10.1038/374227a0) Bourke AFG. 2011 An expanded view of social evolution. In Principles of social evolution, pp. 1–27. Oxford Series in Ecology and Evolution. Oxford, UK: Oxford University Press. Wilson EO. 1971 The insect societies. Harvard, MA: Harvard University Press. Costa JT. 2006 The other insect societies. Cambridge, MA: Harvard University Press. Krause J, Ruxton GD. 2002 Living in groups. Oxford Series in Ecology and Evolution. Oxford, UK: Oxford University Press. Schmid-Hempel P. 1998 Parasites in social insects. Princeton, NJ: Princeton University Press. Cremer S, Armitage SAO, Schmid-Hempel P. 2007 Social immunity. Curr. Biol. 17, R693 –R702. (doi:10.1016/j.cub.2007.06.008) Wilson K, Knell R, Boots M, Koch-Osborne J. 2003 Group living and investment in immune defence: an interspecific analysis. J. Anim. Ecol. 72, 133–143. (doi:10.1046/j.1365-2656.2003.00680.x) Hess G. 1996 Disease in metapopulation models: implications for conservation. Ecology 77, 1617–1632. (doi:10.2307/2265556) Cote IM, Poulin R. 1995 Parasitism and group size in social animals: a meta-analysis. Behav. Ecol. 6, 159–165. (doi:10.1093/beheco/6.2.159) Rifkin JL, Nunn CL, Garamszegi LZ. 2012 Do animals living in larger groups experience greater parasitism? A meta-analysis. Am. Nat. 180, 70– 82. (doi:10.1086/666081) Patterson JEH, Ruckstuhl KE. 2013 Parasite infection and host group size: a meta-analytical review. Parasitology 140, 803–813. (doi:10.1017/ S0031182012002259) Pie MR, Rosengaus RB, Traniello JFA. 2004 Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects. J. Theor. Biol. 226, 45 –51. (doi:10.1016/j. jtbi.2003.08.002) Otterstatter MC, Thomson JD. 2007 Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. Oecologia 154, 411–421. (doi:10.1007/s00442-007-0834-8) Stroeymeyt N, Pe´rez BC, Cremer S. 2014 Organisational immunity in social insects. Curr. Opin. Insect Sci. 5, 1–15. (doi:10.1016/j.cois.2014.09.001) Beckage NE. 2008 Insect immunology. Oxford, UK: Elsevier Inc. De Roode JC, Lefe`vre T. 2012 Behavioral immunity in insects. Insects 3, 789–820. (doi:10.3390/ insects3030789)

8

rstb.royalsocietypublishing.org

Acknowledgements. I thank Peter Kappeler and Charles Nunn for the oppor-

P. Kohlmeier, J. Kramer, Y. Moret, C. Nunn, J. Wong and three anonymous reviewers for their insightful comments on the manuscript. Funding statement. This work has been financed by the German Research Foundation (DFG, ME4179/3-1). Conflict of interests. I have no competing interests.

Downloaded from http://rstb.royalsocietypublishing.org/ on May 22, 2015

58.

59.

61.

62.

63.

64.

65.

66.

67.

68.

69.

70.

71.

72.

73.

74.

75.

76.

77.

78.

79.

80.

81.

82.

83.

84.

85.

86.

carpocapsae. J. Invertebr. Pathol. 95, 17 –25. (doi:10.1016/j.jip.2006.11.004) Weiß C, Kramer J, Holla¨nder K, Meunier J. 2014 Influences of relatedness, food deprivation, and sex on adult behaviors in the group-living insect Forficula auricularia. Ethology 120, 923–932. (doi:10.1111/eth.12261) Starks PT, Blackie CA, Seeley TD. 2000 Fever in honeybee colonies. Naturwissenschaften 87, 229–231. (doi:10.1007/s001140050709) Stahlschmidt ZR, Adamo SA. 2013 Context dependency and generality of fever in insects. Naturwissenschaften 100, 691–696. (doi:10.1007/ s00114-013-1057-y) Heinze J, Walter B. 2010 Moribund ants leave their nests to die in social isolation. Curr. Biol. 20, 249–252. (doi:10.1016/j.cub.2009.12.031) Rosengaus RB, Jordan C, Lefebvre ML, Traniello JFA. 1999 Pathogen alarm behavior in a termite: a new form of communication in social insects. Naturwissenschaften 86, 544–548. (doi:10.1007/ s001140050672) Rosengaus RB, Traniello JFA. 2001 Disease susceptibility and the adaptive nature of colony demography in the dampwood termite Zootermopsis angusticollis. Behav. Ecol. Sociobiol. 50, 546 –556. (doi:10.1007/s002650100394) Royce LA, Rossignol PA, Burgett DM, Stringer BA. 1991 Reduction of tracheal mite parasitism of honey bees by swarming. Phil. Trans. R. Soc. Lond. B 331, 123–129. (doi:10.1098/rstb.1991.0003) Reber A, Castella G, Christe P, Chapuisat M. 2008 Experimentally increased group diversity improves disease resistance in an ant species. Ecol. Lett. 11, 682–689. (doi:10.1111/j.1461-0248.2008.01177.x) Tarpy DR, Seeley TD. 2006 Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous versus monandrous queens. Naturwissenschaften 93, 195–199. (doi:10.1007/ s00114-006-0091-4) Franklin MT, Ritland CE, Myers JH, Cory JS. 2012 Multiple mating and family structure of the western tent caterpillar, Malacosoma californicum pluviale: impact on disease resistance. PLoS ONE 7, e37472. (doi:10.1371/journal.pone.0037472) Sirvio¨ A, Gadau J, Rueppell O, Lamatsch D, Boomsma JJ, Pamilo P, Page RE. 2006 High recombination frequency creates genotypic diversity in colonies of the leaf-cutting ant Acromyrmex echinatior. J. Evol. Biol. 19, 1475 –1485. (doi:10. 1111/j.1420-9101.2006.01131.x) Moreau SJM. 2013 ‘It stings a bit but it cleans well’: venoms of Hymenoptera and their antimicrobial potential. J. Insect Physiol. 59, 186–204. (doi:10. 1016/j.jinsphys.2012.10.005) Otti O, Tragust S, Feldhaar H. 2014 Unifying external and internal immune defences. Trends Ecol. Evol. 29, 625 –634. (doi:10.1016/j.tree.2014.09.002) Jackson DE, Hart AG. 2009 Does sanitation facilitate sociality? Anim. Behav. 77, e1–e5. (doi:10.1016/j. anbehav.2008.09.013) Wong JWY, Meunier J, Ko¨lliker M. 2013 The evolution of parental care in insects: the roles of

9

Phil. Trans. R. Soc. B 370: 20140102

60.

(eds JC Choe, BJ Crespi), pp. 26 –51. Cambridge, UK: Cambridge University Press. Kirkendall LR, Kent DS, Raffa KF, Kents DS. 1997 Interactions among males, females and offspring in bark and ambrosia beetles: the significance of living in tunnels for the evolution of social behavior. In The evolution of social behavior in insects and arachnids (eds JC Choe, BJ Crespi), pp. 181–215. Cambridge, UK: Cambridge University Press. West MJ, Alexander RD. 1963 Sub-social behavior in a burrowing cricket, Anurogryllus muticus (De Geer). Ohio J. Sci. 63, 19 –24. Tanaka Y, Kasuya E. 2011 Flying distance of frass kicked by the grasshopper Atractomorpha lata and factors affecting the flying distance. Entomol. Sci. 14, 133– 141. (doi:10.1111/j.1479-8298.2010. 00427.x) Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, Cremer S. 2013 Ants disinfect fungusexposed brood by oral uptake and spread of their poison. Curr. Biol. 23, 76 –82. (doi:10.1016/j.cub. 2012.11.034) Ilyasov RA, Gaifullina LR, Saltykova ES, Poskryakov AV, Nikolaenko AG. 2013 Defensins in the honeybee antiinfectious protection. J. Evol. Biochem. Physiol. 49, 1 –9. (doi:10.1134/S0022093013010015) Strohm E, Linsenmair KE. 2001 Females of the European beewolf preserve their honeybee prey against competing fungi. Ecol. Entomol. 26, 198 –203. (doi:10.1046/j.1365-2311.2001.00300.x) Bos N, Lefe`vre T, Jensen AB, D’Ettorre P. 2012 Sick ants become unsociable. J. Evol. Biol. 25, 342– 351. (doi:10.1111/j.1420-9101.2011.02425.x) Ugelvig LV, Cremer S. 2007 Social prophylaxis: group interaction promotes collective immunity in ant colonies. Curr. Biol. 17, 1967–1971. (doi:10. 1016/j.cub.2007.10.029) Ugelvig LV, Kronauer DJC, Schrempf A, Heinze J, Cremer S. 2010 Rapid anti-pathogen response in ant societies relies on high genetic diversity. Proc. R. Soc. B 277, 2821 –2828. (doi:10.1098/rspb. 2010.0644) Arathi HS, Burns I, Spivak M. 1999 Ethology of hygienic behaviour in the honey bee Apis mellifera L. (Hymenoptera: Apidae): behavioural repertoire of hygienic bees. Ethology 106, 365–379. (doi:10. 1046/j.1439-0310.2000.00556.x) Moret Y, Schmid-Hempel P. 2001 Immune defence in bumble-bee offspring. Nature 414, 506. (doi:10. 1038/35107138) McLean AHC, Arce AN, Smiseth PT, Rozen DE. 2014 Late-life and intergenerational effects of larval exposure to microbial competitors in the burying beetle Nicrophorus vespilloides. J. Evol. Biol. 27, 1205 –1216. (doi:10.1111/jeb.12394) Konrad M et al. 2012 Social transfer of pathogenic fungus promotes active immunisation in ant colonies. PLoS Biol. 10, e1001300. (doi:10.1371/ journal.pbio.1001300) Wilson-Rich N, Stuart RJ, Rosengaus RB. 2007 Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema

rstb.royalsocietypublishing.org

43. Baracchi D, Mazza G, Turillazzi S. 2012 From individual to collective immunity: the role of the venom as antimicrobial agent in the Stenogastrinae wasp societies. J. Insect Physiol. 58, 188 –193. (doi:10.1016/j.jinsphys.2011.11.007) 44. Cardoza YJ, Klepzig KD, Raffa KF. 2006 Bacteria in oral secretions of an endophytic insect inhibit antagonistic fungi. Ecol. Entomol. 31, 636– 645. (doi:10.1111/j.1365-2311.2006.00829.x) 45. Kaltenpoth M, Go¨ttler W, Herzner G, Strohm E. 2005 Symbiotic bacteria protect wasp larvae from fungal infestation. Curr. Biol. 15, 475–479. (doi:10.1016/j. cub.2004.12.084) 46. Rosengaus RB, Guldin MR, Traniello JFA. 1998 Inhibitory effect of termite fecal pellets on fungal spore germination. J. Chem. Ecol. 24, 1697– 1706. (doi:10.1023/A:1020872729671) 47. Chouvenc T, Efstathion CA, Elliott ML, Su N. 2013 Extended disease resistance emerging from the faecal nest of a subterranean termite. Proc. R. Soc. B 280, 20131885. (doi:10.1098/rspb.2013.1885) 48. Koch H, Schmid-Hempel P. 2011 Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl Acad. Sci. USA 108, 19 288–19 292. (doi:10.1073/pnas. 1110474108) 49. Rosengaus RB, Mead K, Du Comb WS, Benson RW, Godoy VG. 2013 Nest sanitation through defecation: antifungal properties of wood cockroach feces. Naturwissenschaften 100, 1051–1059. (doi:10. 1007/s00114-013-1110-x) 50. Cotter SC, Kilner RM. 2010 Sexual division of antibacterial resource defence in breeding burying beetles, Nicrophorus vespilloides. J. Anim. Ecol. 79, 35 –43. (doi:10.1111/j.1365-2656.2009.01593.x) 51. Steiger S, Gershman SN, Pettinger AM, Eggert A-K, Sakaluk SK. 2011 Sex differences in immunity and rapid upregulation of immune defence during parental care in the burying beetle, Nicrophorus orbicollis. Funct. Ecol. 25, 1368 –1378. (doi:10.1111/ j.1365-2435.2011.01895.x) 52. Reavey CE, Beare L, Cotter SC. 2014 Parental care influences social immunity in burying beetle larvae. Ecol. Entomol. 39, 395–398. (doi:10.1111/ een.12099) 53. Arce AN, Smiseth PT, Rozen DE. 2013 Antimicrobial secretions and social immunity in larval burying beetles, Nicrophorus vespilloides. Anim. Behav. 86, 741–745. (doi:10.1016/j.anbehav.2013.07.008) 54. Diez L, Deneubourg J-L, Detrain C. 2012 Social prophylaxis through distant corpse removal in ants. Naturwissenschaften 99, 833 –842. (doi:10.1007/ s00114-012-0965-6) 55. Bot ANM, Currie CR, Hart AG, Boomsma JJ. 2001 Waste management in leaf-cutting ants. Ethol. Ecol. Evol. 13, 225 –237. (doi:10.1080/08927014.2001. 9522772) 56. Weiss MR. 2006 Defecation behavior and ecology of insects. Annu. Rev. Entomol. 51, 635–661. (doi:10. 1146/annurev.ento.49.061802.123212) 57. Nalepa CA, Bell WJ. 1997 Postovulation parental investment and parental care in cockroaches. In The evolution of social behavior in insects and arachnids

Downloaded from http://rstb.royalsocietypublishing.org/ on May 22, 2015

88.

90.

91.

92.

93.

94.

104.

105.

106. 107.

108.

109.

110.

111.

112.

Sociobiol. 66, 791–796. (doi:10.1007/s00265-0121327-2) Wang Y, Yang P, Cui F, Kang L. 2013 Altered immunity in crowded locust reduced fungal (Metarhizium anisopliae) pathogenesis. PLoS Pathog. 9, e1003102. (doi:10.1371/journal.ppat.1003102) Miller GA, Simpson SJ. 2010 Isolation from a marching band increases haemocyte density in wild locusts (Chortoicetes terminifera). Ecol. Entomol. 35, 236–239. (doi:10.1111/j.1365-2311.2010.01180.x) Stearns SC. 1992 The evolution of life histories. Oxford, UK: Oxford University Press. Van Noordwijk AJ, de Jong G. 1986 Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137–142. (doi:10.1086/284547) Zhukovskaya M, Yanagawa A, Forschler B. 2013 Grooming behavior as a mechanism of insect disease defense. Insects 4, 609 –630. (doi:10.3390/ insects4040609) Ratnieks FLW, Foster KR, Wenseleers T. 2006 Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581 –608. (doi:10.1146/annurev.ento.51. 110104.151003) Myerscough MR, Oldroyd BP. 2004 Simulation models of the role of genetic variability in social insect task allocation. Insectes Soc. 51, 146– 152. (doi:10.1007/s00040-003-0713-1) Pull CD, Hughes WOH, Brown MJF. 2013 Tolerating an infection: an indirect benefit of co-founding queen associations in the ant Lasius niger. Naturwissenschaften 100, 1125 –1136. (doi:10. 1007/s00114-013-1115-5) Ko¨lliker M. 2007 Benefits and costs of earwig (Forficula auricularia) family life. Behav. Ecol. Sociobiol. 61, 1489–1497. (doi:10.1007/s00265-007-0381-7)

10

Phil. Trans. R. Soc. B 370: 20140102

89.

95. Reber A, Purcell J, Buechel SD, Buri P, Chapuisat M. 2011 The expression and impact of antifungal grooming in ants. J. Evol. Biol. 24, 954 –964. (doi:10.1111/j.1420-9101.2011.02230.x) 96. Wilson K, Cotter SC. 2009 Density-dependent prophylaxis in insects. In Phenotypic plasticity of insects (eds DW Whitman, TN Ananthakrishnan), pp. 137–176. CRC Press. 97. Babayan SA, Schneider DS. 2012 Immunity in society: diverse solutions to common problems. PLoS Biol. 10, e1001297. (doi:10.1371/journal.pbio. 1001297) 98. Hoggard SJ, Wilson PD, Beattie AJ, Stow A. 2011 Social complexity and nesting habits are factors in the evolution of antimicrobial defences in wasps. PLoS ONE 6, e21763. (doi:10.1371/journal.pone.0021763) 99. Stow A, Briscoe D, Gillings M, Holley M, Smith S, Leys R, Silberbauer T, Turnbull C, Beattie A. 2007 Antimicrobial defences increase with sociality in bees. Biol. Lett. 3, 422–424. (doi:10.1098/rsbl. 2007.0178) 100. Turnbull C et al. 2011 Antimicrobial strength increases with group size: implications for social evolution. Biol. Lett. 7, 249–252. (doi:10.1098/rsbl. 2010.0719) 101. Wilson K, Thomas MB, Blanford S, Doggett M, Simpson SJ, Moore SL. 2002 Coping with crowds: density-dependent disease resistance in desert locusts. Proc. Natl Acad. Sci. USA 99, 5471–5475. (doi:10.1073/pnas.082461999) 102. Weinstock GM et al. 2006 Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931–949. (doi:10.1038/nature05260) 103. Richter J, Helbing S, Erler S, Lattorff HMG. 2012 Social context-dependent immune gene expression in bumblebees (Bombus terrestris). Behav. Ecol.

rstb.royalsocietypublishing.org

87.

ecology, life history and the social environment. Ecol. Entomol. 38, 123– 137. (doi:10.1111/een. 12000) Boomsma JJ, Schmid-Hempel P, Hughes WOH. 2005 Life histories and parasite pressure across the major groups of social insects. In Insect evolutionary ecology (eds M Fellowes, G Holloway, J Rolff ), pp. 139–175. Wallingford: CABI. Bell WJ, Roth LM, Nalepa CA. 2007 Cockroaches: ecology, behavior, and natural history. Baltimore, MD: The Johns Hopkins University Press. Van Baalen M, Beekman M. 2006 The costs and benefits of genetic heterogeneity in resistance against parasites in social insects. Am. Nat. 167, 568–577. (doi:10.1086/501169) Evans JD et al. 2006 Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645–656. (doi:10.1111/j.1365-2583. 2006.00682.x) Rueppell O, Meier S, Deutsch R. 2012 Multiple mating but not recombination causes quantitative increase in offspring genetic diversity for varying genetic architectures. PLoS ONE 7, e47220. (doi:10. 1371/journal.pone.0047220) Bru¨tsch T, Felden A, Reber A, Chapuisat M. 2014 Ant queens (Hymenoptera: Formicidae) are attracted to fungal pathogens during the initial stage of colony founding. Myrmecol. News 20, 71 –76. Pontieri L, Vojvodic S, Graham R, Pedersen JS, Linksvayer TA. 2014 Ant colonies prefer infected over uninfected nest sites. PLoS ONE 9, e111961. (doi:10.1371/journal.pone.0111961) Rosengaus RB, James L-T, Hartke TR, Brent CS. 2011 Mate preference and disease risk in Zootermopsis angusticollis (Isoptera: Termopsidae). Environ. Entomol. 40, 1554 –1565. (doi:10.1603/EN11055)