Evolutionary feedbacks between insect sociality and microbial management

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Peter HW Biedermann1,2 and Marko Rohlfs3,4 Fitness-determining interactions with microbes — in particular fungi — have often been considered a by-product of social evolution in insects. Here, we take the view that both beneficial and harmful microbial consortia are major drivers of social behaviours in many insect systems — ranging from aggregation to eusociality. We propose evolutionary feedbacks between the insect sociality and microbial communities that strengthen mutualistic interactions with beneficial (dietary or defensive) microbes and simultaneously increase the capacity to defend against pathogens (i.e. social immunity). We identified variation in habitat stability — as determined by breeding site predictability and ephemerality — as a main ecological factor that constrains these feedbacks. To test this hypothesis we suggest following the evolution of insect social traits upon experimental manipulation of habitat stability and microbial consortia. Addresses 1 Department of Biochemistry, Max-Planck-Institute for Chemical Ecology, Jena, Germany 2 Institute for Animal Ecology and Tropical Biology, Julius-MaximiliansUniversity of Wu¨rzburg, Germany 3 University of Bremen, Institute of Ecology, Population- and Evolutionary Ecology Group, Germany 4 University of Goettingen, J.F. Blumenbach Institute of Zoology, Animal Ecology Group, Germany Corresponding authors: Biedermann, Peter HW (p[emailprotected]) and Rohlfs, Marko ([emailprotected])

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doi:10.1016/j.cois.2017.06.003

[3,4,5]. The tricky part is that keeping the ‘harmfuls’ in check and propagating the ‘beneficials’ often need to be accomplished simultaneously (Box 1). In this article, we argue that social interactions between insects — from simple collective feeding to complex division of labour (Figure 1) — provide strong means to construct highquality microbial environments for insect fitness by selectively favouring the beneficial microbes, while keeping the harmful microbes suppressed.

Coevolution of insect sociality and beneficial microbes Insects show a fascinating array of behaviours (Figure 1) that promote beneficial microbes in their vicinity [4,10–13]. If the collective execution of these behaviours further improves the growth of the beneficials. This can start a positive evolutionary feedback process between the partners; every amelioration in the social selection and propagation of these microbes may feed back on insect fitness, with the potential of tightening the insect–microbe mutualism even more (Figure 2a). Interestingly, this process may speed up during this co-evolution as within species relatedness is expected to increase, which reinforces investments in the mutualism as the benefits are likely to profit relatives [14]. In the end, kin selection in combination with the proposed feedback may lead to the highest level of interspecific and intraspecific cooperation, namely obligate mutualism in the context of insect eusociality. In fungus-farming ant and termite societies, for example, characterized by a complex caste system, millions of workers and just a few reproductive individuals fully rely on each other and their farmed fungus for subsistence [13]. However, as pointed out by Korb [15], crucial experimental tests that allow differentiation between direct and indirect fitness gains of collective behaviours are still scarce.

2214-5745/# 2017 Published by Elsevier Inc.

Coevolution of insect sociality and harmful microbes

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Social management of microbes by insects Since their evolutionary origin insects co-occur with microorganisms (e.g. [1,2]). The resulting interactions range from harmful to beneficial. Insects have evolved a strikingly diverse array of behavioural and physiological strategies both to combat microbial pathogens, parasites or competitors and to effectively transmit and promote those microbes that benefit them as essential dietary supplements, substrate degraders, or defence agents www.sciencedirect.com

The success of insect–microbe mutualisms is frequently challenged by invasion of non-beneficial microbes that harm either the insects (e.g. as pathogens, parasites or toxin-producers) or their beneficial microbial partners (e.g. as pathogens or resource-competitors). Insects have evolved the neurophysiological ability to identify such microbial threats and various strategies to prevent establishment of harmful microbes in their habitats, ranging from simple avoidance of infested habitats [16] to physical, for example, grooming, weeding [17], or chemical suppression of microbial invaders [18,19] (Figure 1). Like for beneficial microbes, we argue that collective Current Opinion in Insect Science 2017, 22:1–9

Please cite this article in press as: Biedermann PHW, Rohlfs M: Evolutionary feedbacks between insect sociality and microbial management, Curr Opin Insect Sci (2017), http://dx.doi.org/10.1016/ j.cois.2017.06.003

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2 Social insects

Glossary Cooperation: exchange of beneficial traits between partners of the same or different species, which increases the direct fitness of each partner Symbiosis: a close and often long-term interaction between two different species, which makes no statement about the fitness effects and thus includes mutualism, commensalism and antagonism Sociality: behavioural interactions between partners of the same species, which are often related, thereby increasing the inclusive fitness of each partner Interspecific mutualism: exchange of beneficial traits between partners of different species, thereby increasing the direct fitness of each partner Collective behaviour (= Semisociality): aggregation of mostly unrelated individuals of the same species, which are usually driven by direct fitness gains Parental care (= Subsociality): behavioural investment of the parents into the direct fitness of their offspring Facultative eusociality: social organization defined by overlapping offspring generations and helping offspring that is capable of own reproduction but partly refrains to do so Obligate eusociality: social organization defined by overlapping offspring generations and presence of morphologically specialized castes of workers and reproductives Co-evolution: selective pressures between species or traits that are reciprocally exerted, thereby affecting each other’s evolution Vertical transmission: passing of symbiont from parents to offspring Horizontal transmission: uptake of symbiont from the environment Partner choice: preferential interaction with a beneficial subset of partners. Choice can be made in response to honest signalling of partner quality or by imposing a cost to partners to screen out cooperators Sanctions (= Policing): imposing a penalty on a non-cooperative partner Partner-fidelity feedback: improvement of the fitness of a partner of the same or different species, which improves its phenotypic ability to return the aid Kin selection: form of natural selection that favours behaviour, which may decrease an individual’s direct fitness but benefits that of their kin (who share a proportion of their genes)

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behaviours can reinforce the efficacy of individual strategies to suppress harmful microbes via density or groupmediated effects, which has often been termed ‘social immunity’ [19,20]. However, in contrast to the common view in the social immunity literature where pathogen defence is regarded as a necessary consequence of increased transmission of pathogens in genetically homogenous family groups, we propose that harmful microbes are a major driver of social evolution in some insects. A feedback loop can be started if, for example, members of a social group profit from the joint suppression of detrimental microbes and are thus selected for staying and helping even more, which again feeds back to an improved suppression of microbes (Figure 2b). Understanding the origin and courses of such feedback loops requires studying facultative eusocial and non-eusocial insect systems.

Constraints on the evolution of stable mutualism and social complexity Despite the advantages of cooperation, both sociality and mutualism have remained rudimentary in many insect– Current Opinion in Insect Science 2017, 22:1–9

Box 1 Social means of selecting and maintaining beneficial microbes How do insects choose and maintain the beneficial over the harmful microbes? This is not trivial, as for insects the qualities of the microbes are often hidden (i.e. costly signalling by the microbes is rare; but see examples for mutualist selection in Figure 1 [6,7,8]) and all potential partners would benefit from being chosen, so even the pathogens have no interest in revealing their true intention [9]. We identified four potential mechanisms that are often socially mediated and thus expected to increase in efficiency during social evolution (Figure 1): First, screening beneficial and harmful microbes by the insects through creation of a group-mediated filtering environment that excludes all but the highest-quality partners (e.g. collective feeding and application of defences). Second, direct collective defence against harmful microbes and sanctioning of cheaters. Third, vertical transmission of beneficial microbes within a social group from adults to offspring, which leads to partner fidelity and thus aligns fitness interests of insects and microbes. Fourth, groupmediated habitat stability and maintenance also leading to prolonged contact and partner fidelity.

microbe systems. We suggest that the evolution of more complex social behaviours may be ecologically constrained, predominantly by habitat instability and insect population structure, that is, whether generations overlap and interact, or whether parental and offspring generations are largely discrete and hardly interact. Interestingly, with the transition to eusociality, insects managed to disengage almost completely from these constraints by creating their own habitat [21] (Figure 1). This also relates to regulating microbial communities to support colonial life, such as food-fungus in farming systems. In the following, we illustrate our idea of a common feedback between the social behaviour of insects and their association with microbes by focusing mainly on different insect–fungus systems. Despite the focus on insects and fungi, we note that our ideas should be generally applicable to other animal–fungus or insect–bacteria mutualisms and antagonisms.

Examples of collective fungal management at different levels of sociality Habitat instability prevents the microbe managementsociality feedback loop to run its course in Drosophila fruit flies

Semisocial aggregation is particularly frequent in insects exploiting ephemeral resources, for example dung, carrion, fruits, for larval development (Figure 1). In the Drosophila model system, aggregation of unrelated individuals is found across distinct breeding patches, often through pheromone-mediated clumping of adults [22], and within patches through mutual attraction of larvae [23]. Aggregative egg-laying and larval foraging has been related to first, the suppression of detrimental mould fungi, such as Aspergillus sp., Penicillium sp. (e.g. [24– 26]), and second, the transmission and propagation of beneficial yeasts and bacteria [27,28]. Collective larval www.sciencedirect.com

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Figure 1

Semisocial aggregation

Beneficial microorganisms

Examples

Subsocial parental care

Facultative eusociality

Obligate eusociality

Nutritional, defensive fungi and bacteria

Nutritional fungi; defensive bacteria

Nutritional fungi; nutritional, defensive bacteria

Fruit flies

Burying beetles

Ambrosia beetles

Attine ants

Food competitors, insect pathogens

Substrate competitors, insect and fungal pathogens

(Drosophila melanogaster, Nicrophorus vespilloides, Xyleborinus saxesenii, Atta cephalotes)

Harmful microorganisms Selective feeding1

Collective feeding2

(+)

–

Division of labor

–

(+)

Mutualist selection6

(+)

Immunity transfer

–

Animal cadavers

Freshly deadwood

Direct management

Vertical transm.4 Parental care Alloparental care5

Habitat Habitat stability Other examples for similar social syndromes

Rotting fruits poor •Houseflies •Sciarid flies •probably many more

Nests underground, fresh leaves etc. as substrate high

•Many beetle families •Gall midges •Earwigs •Cryptocercus roaches

•Some mites

•Fungus-farming termites •Lower termites •Some stingless bees

Current Opinion in Insect Science

Social management of beneficial and harmful microorganims in four examples along the transition from semisociality to eusociality. Given are the beneficial and harmful microbes for each Drosophila melanogaster (Photo credit: M. Trienens), Nicrophorus vespilloides (Photo credit: S. Steiger), Xyleborinus saxesenii (Photo credit: P. Biedermann), and Atta cephalotes (Photo credit: G. Kunz) as well as the most important socially mediated behaviours used by these insects to structure their microbial communities. Habitat stability is the most important mediator of social evolution in these systems and is mainly limited by pathogens and the ephemerality of the food resources. 1 — Selective feeding can lead to frequency dependent selection of beneficials; 2 — collective feeding can lead to only beneficials surviving and can help overcoming fungal defenses; 3 — direct management of microbes by specialized behaviours or application of secretions or symbionts; 4 — vertical transmission of microbes between parents and offspring leads to linked fitness with host, which facilitates mutualism with beneficials and lowers virulence of pathogens; 5 — alloparental care stands for adult offspring caring for relatives; 6 — shown recognition of mutualistic cultivars and defensive bacteria can be used, for example, by ants to select more beneficial strains even within a lifetime of a nest.

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attack of mould colonies [29] can slow-down the expansion of toxin-producing fungal hyphae (Figure 2a) and thereby benefits individual Drosophila larvae in larger groups [30]. However, fly larvae achieve more sustainable management of moulds in the presence of yeasts and bacteria [25,31,32]. Besides being superior competitors for nutrients, insect-transmitted yeasts and yeast/bacteria www.sciencedirect.com

communities are likely to produce metabolites that have anti-mould properties [33,34]. Additionally, yeasts (and probably bacteria) are essential for Drosophila development in an otherwise nutrient-poor substrate (e.g. [27,35]). Yeast species, however, differ in their beneficial effect on the generalist fruit fly Drosophila Current Opinion in Insect Science 2017, 22:1–9

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Figure 2

(a) Proposed sociality - mutualism feedback

(b) Proposed sociality - pathogenicity feedback frequent host-microbe interaction

Selection

Host-pathogen arms race Genetic change in pathogen counters new host defense

Evolution of mutualism Genetic change in host and microbial traits that tighten the mutualism and lower the conflict

Increased investment of host increases microbe fitness

Habitat stability (pathogens)

Increased investment of microbes increases host fitness

Selection

Evolution of sociality Genetic change in traits that tighten social structure and lower conflict

Selection

Evolution of pathogen defense Genetic change in host traits that lower pathogen pressure

Better defense of host decreases microbe fitness

Habitat stability (food resources)

Better defense increases host fitness

Selection

Evolution of sociality Genetic change in traits that tighten social structure and lower conflict Current Opinion in Insect Science

A representation of the possible feedback mechanisms between the evolution of insect social behaviour and insect–microbe mutualisms (a) as well as insect–pathogen interactions (b). Both feedback loops are largely driven by the stability of the habitat for maintaining the insect–microbe association. The two levels of arrows denote possible evolution of new modes of management (yellow to red; e.g. evolution of a new defensive behaviour) and strengthening existing modes of microbial management (small to large; e.g. increasing amounts of defensive secretions). (a) Given a long-lived habitat (relative to the lifetime of an insect and primarily threatened by pathogen pressure), frequent host-microbe interactions and mechanisms to control intraspecific and interspecific conflict (i.e. positive assortment), selection on social host traits that profit their beneficial microbial partners alters the environment of the microbes, resulting in a change of their fitness landscape and influencing selection on their genes (i.e. evolution of interspecific mutualism). This, in turn, increases the benefit of the microbes for their social hosts by lowering within-group conflict Q6 in the host, that is, competition for food, and influences selection on heritable traits that facilitate evolution of intraspecific sociality [80]. (b) Frequent interactions between insect host and harmful microbes (i.e. pathogens, competitors) selects for social defenses in host (i.e. evolution of pathogen defense), which can increase host fitness. If there are enough food resources (= major factor of habitat stability in this case) to maintain a larger social group this can lead to more complex division of labour (i.e. evolution of sociality), which again results in better defense against harmful microbes. This either leads to the elimination of the microbe or — if it frequently interacts with the insect host — selects for counteradaptations in the microbe (i.e. host-pathogen arms race).

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melanogaster [36], and associated yeast communities vary as a function of habitat properties [37] and larval health status, for example, whether they suffer from parasite infestation [38]. This suggests no obligatory association and creates the opportunity for choosing and promoting the most beneficial microbial partners to improve immune and nutritional physiology adaptations. As demonstrated by Stamps et al. [28], choice and propagation of microbial partners may take place during egg-laying when adult Drosophila transmit microbes to offspring feeding sites, and during offspring development when larvae not only consume yeasts but also propagate a specific yeast community. By using different isolates of baker’s yeast, Saccharomyces cerevisiae, Buser et al. [39] provide experimental evidence of a positive feedback between yeast dispersal by D. simulans flies and female reproductive output. Current Opinion in Insect Science 2017, 22:1–9

Although drosophilid semisocial behaviours facilitate an efficient form of microbe management that modifies and stabilizes habitat conditions (Figure 1), the breeding sites themselves (e.g. windfall fruits) are ephemeral and unpredictable in space and time. Poor habitat stability is unlikely to favour a persistent Drosophila–microbe mutualism if insect-mediated growth of beneficial microbes strongly depends on habitat characteristics, for example, different types of fruits or other plant material. Moreover, unstable habitats do not select for tight cross-generational interactions, that is, intensive parental care characterized by the formation of stable family groups and sophisticated modes of microbe transmission. We hypothesize that in Drosophila and ecologically similar systems, habitat instability imposes constraints on the proposed positive evolutionary feedback between microbe management and insect sociality (Figure 2). Because habitat instability www.sciencedirect.com

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causes disintegration of mutualistic interactions with microbes, which outweighs the benefits of more intensive parental care, Drosophila social interactions do not further evolve beyond semisociality and rudimentary subsociality.

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Elaborated parental care in Nicrophorus burying beetles tightens mutualism with microbes

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In contrast to fruit flies, Nicrophorus beetles can secure otherwise unpredictable breeding resources for their offspring by burying small vertebrate carcasses. Even though the resource patch is entirely consumed during one breeding event, burying beetles show intensive subsocial behaviours comprising elaborate carrion manipulation, parental grooming and feeding of larvae [40], which provide substantial benefits to their offspring [41] (Figure 1). As with Drosophila, these behaviours would remain largely ineffective if microorganisms were not involved. Indeed, different microbial partners seem to contribute to protecting the breeding site from harmful bacteria and fungi [42], which are vertically transmitted to offspring via anal secretions adults apply to the carcass surface [43]. Resource preservation also includes the insects’ own immune defence components, for example, antimicrobial peptides [44]. The bacteria and yeasts involved have antimicrobial properties but appear to also predigest the carrion and thereby synthesize essential nutrients that might accelerate larval development [43]. Although biogeographical studies need to determine the extent to which burying beetles, beyond family groups, have evolved mutualisms with specific microbial lineages, this system is a good example of how an increase in habitat stability — created by the insects themselves — links to an apparently stable and functionally important insect–microbe mutualism (Figure 2). Prolonged maintenance of the family group and hence the evolution of more complex social behaviours is, however, constrained by the ephemerality of the carrion resource.

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Division of labour in wood-boring weevils enables fungus farming in semi-stable habitats

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Symbioses with fungi have evolved multiple times independently in bark and ambrosia beetles (Curculionidae: Scolytinae and Platypodinae), typically accompanied by advancements in their social systems [45,46]. These beetles colonize freshly dead wood — a process mediated by noxious plant and microbial volatiles (e.g. ethanol, terpenes [47]). By choosing such an antimicrobial and thus ‘screening’ environment they selectively favour those microbes out of the vertically transmitted symbiont community that are largely insensitive to these toxic compounds, like nutritious ascomycete ambrosia fungi (Ranger & Biedermann, unpublished data). When mothers (or both parents) bore a tunnel system and inoculate the walls with mutualistic fungus spores from their fungus pockets (mycetangium [12,48]), the mutualists of the beetles are favoured over accidentally transmitted www.sciencedirect.com

microbes. This is continued by socially mediated management as toxins in the substrate quickly break down (Figure 1). The establishing fungus community and eggs are constantly monitored by the mother beetle (e.g. [49,50], PHW Biedermann, The evolution of cooperation in ambrosia beetles, PhD thesis, University of Bern, 2012) and fungal pathogens can be initially suppressed by smearing of antibiotic-producing bacteria in oral secretions on pathogen infested areas (in Dendroctonus frontalis [51,52]). More advanced social behaviours are restricted to ambrosia beetles, because their obligate dependence on fungi requires care, thus the mothers continue to interact with the fungus cultures and their offspring even after egghatching (Figure 1 [46,53]). Ambrosia fungi produce nutritious fruiting structures only in the interaction with beetles (PHW Biedermann, The evolution of cooperation in ambrosia beetles, PhD thesis, University of Bern, 2012, [54]) and harmful fungi (entomopathogens, mycopathogens and fungal competitors) are a constant threat [55]. In a few lineages microbial management is only by the mothers, which provision larvae in separate cradles while keeping the entrance tunnels free of pathogens and frass (e.g. Xyloterini, Corthylini, some Platypodinae [46]). On the other hand, in the facultatively eusocial societies of some Xyleborini, parents, immature and adult offspring co-occur in the same tunnels, and microbial management tasks are divided between them (parental and alloparental care) (PHW Biedermann, The evolution of cooperation in ambrosia beetles, PhD thesis, University of Bern, 2012, [53]). Adults can differentiate between the odours of beneficial and harmful fungi [56,57] and both adults and larvae suppress the growth of fungal pathogens in vitro ([53], JA Nuotcla, Defence mechanisms against pathogenic fungi in the ambrosia beetle Xyleborinus saxesenii, MSc thesis, Institute of Ecology & Evolution, University of Bern, 2015), while inducing fruiting structures in their ambrosia fungi [54]. The mechanistic basis for both phenomena is unknown and might involve either bioactive secretions or defensive/promoting microbes [5,52,58,59]. Beetles also smear larval faeces on the tunnel walls to fertilize ambrosia fungus beds [60] and possibly also to re-inoculate fungal spores. Overall, this socially mediated promotion of the beneficial fungi and defence against pathogens best explains why the fungus and thus beetle productivity boost after a threshold of about ten to twenty larval and adult workers is reached [61]. The limiting factor in ambrosia beetle social evolution is deterioration of the habitat. Subsocial species typically breed in small wood resources like twigs or small diameter trees, whereas facultatively eusocial species colonize large diameter resources and the only obligately eusocial species breeds in living trees [46,62]. More long-lived resources allow multiple generations to develop within Current Opinion in Insect Science 2017, 22:1–9

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one nest and thus a positive evolutionary feedback between sociality and mutualism. As beetles directly induce the fruiting of their ambrosia fungi, the more beetles there are the more productive is the fungus (Figure 2a). A necessary requirement for this feedback is the control of pathogens, however. In ambrosia beetles this has likely been another driving factor of sociality (Figure 2b). An experiment with artificial Xyleborinus saxesenii nests revealed that injection of entomopathogenic Aspergillus sp. spores tends to delay adult-offspring dispersal from the natal nest and significantly enhances their allogrooming behaviour, indicating that the presence of the pathogen facilitates social behaviour and reduces dispersal to breed independently (JA Nuotcla, Defence mechanisms against pathogenic fungi in the ambrosia beetle Xyleborinus saxesenii, MSc thesis, Institute of Ecology & Evolution, University of Bern, 2015). This means that social management of cultivars can both enhance food productivity, which may entice offspring to stay at the nest and cooperate. Highly stable agricultural societies of attine ants enabled by full control over microbes

Another group of fungus-farming insects — the attine ants — already lived in obligately eusocial societies when they evolved their mutualism with Leucocoprinae fungi about 50 million years ago [4,63]. From the beginning attine-ant fungiculture is a multipartite relationship, because the cultivar fungus is threatened by a mycopathogen in the genus Escovopsis, which is mostly defended by an antibiotic-producing actinomycete bacterium in the genus Pseudonocardia that is growing on the ants’ integuments [4,64]. Apart from application of this defensive mutualist, in the higher attines, up to twelve different worker morphs use an array of behavioural and chemical defences against pathogens, from weeding and grooming [17] involving antibiotic secretions from their metapleural glands (e.g. [65]) to compartmentalization of gardens for isolation of contaminated areas [66] and removing of waste and cadavers (Figure 1 [19]). Cultivar fungi, on the other hand, are constantly provisioned with new substrate (which has passed several castes for disinfection) and are induced to produce nutritional fruiting structures (termed gongylidia) only in the presence of ants (like for ambrosia fungi the underlying mechanism is unknown [7]). Workers have been also shown to recognize both their beneficial cultivar and the native Pseudonocardia strain [4,8], which allow them to artificially select for the best mutualists even within the lifetime of an ants’ nest. Only by collectively managing both harmful and beneficial microbes, can attine ants stabilize their agriculture for decades. In evolutionary terms, a stable habitat has helped to strengthen the feedback between the ants’ social tasks and the mutualism (Figure 2a), but has also led to an evolutionary arms race between the ants’ social Current Opinion in Insect Science 2017, 22:1–9

Box 2 Fungus farming is possible in solitary species, but only in near pathogen-free habitats Obligate mutualisms with farmed fungi evolved in at least three nonsocial insect lineages — wood wasps (WW; Hymenoptera: Siricidae), ship-timber beetles (STB; Coleoptera: Lymexylidae) and lizard beetles (LB; Coleoptera: Erotylidae) [12,67]. In all these systems yeast-like fungi are ‘farmed’ by solitary larvae in tunnels within wood (WW, STB) or in internode cavities of bamboo (LB). These habitats are near-sterile when settled by the insects and are completely sealed off from the environment immediately after colonization. Also common to all is the smearing of eggs with the beneficial yeasts from a mycetangium at the female ovipositor and a mechanism of inoculation of the substrate that excludes other (harmful) microbes. Of course, there are cases in these systems when pathogens enter and destroy single larvae, but in general harmful microbes are mostly absent. Thus, the habitat is stable and partner fidelity feedback between insects and yeasts can select for mutualism even in the absence of social management of microbes. Therefore, these solitary farmers have managed to disengage from habitat constraints imposed by pathogens in complete absence of social immunity.

defences, their mutualistic bacteria and a specialized fungus pathogen (Figure 2b). What remains poorly studied is the evolutionary feedback between advancements in the morphological division of labour and key inventions in both the cultivars (e.g. nutritional fruiting of farmed fungi) and pathogens (e.g. development of resistance against antibiotics).

Ship-timber beetle, Hylocoetes dermestoides (Lymexylidae) (Photo credit: G. Holighaus)

Conclusion The transition from a predominantly solitary to a predominantly social lifestyle in insects is thought to create new challenges with detrimental microbes, for example, increased parasite infection [19,20]. Here we pose the hypothesis that major aspects of insect social behaviours have evolved in response to some pertinent challenges related to living in a microbial environment that can be both beneficial and harmful. The different stages and transitions of fungal-mediated social behaviours can be seen in the different insect systems reviewed in this article. Lineage-specific developmental, morphological, reproductive and neurobiological traits likely constrain the evolution of social behaviours, yet habitat stability is the prevailing ecological factor that sets the fitness payoff of heritable variation in social complexity [68,69]. Independent of the habitat characteristics, collective transmission/cultivation of beneficial microbes and suppression of ubiquitous and destructive fungi entails large direct fitness benefits to the individual. We thus argue that in such systems indirect fitness benefits (due to kin-selection) could be of minor importance for social behaviours to evolve and to elaborate (as seen in the most complex eusociality of attine ants) as currently assumed. However, www.sciencedirect.com

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because management of fungal communities is often inherently linked to family groups/societies, careful experiments are needed to test this assumption [15]. Moreover, we think that some easily manipulable insect systems (e.g. Drosophila flies, ambrosia beetles) can be used to explore experimentally the extent to which variation in fungal communities and their functional traits feed back with habitat properties, selecting for more intensive and diverse social behaviours in insects. Our proposed opinion needs to be challenged by answering following questions: - Can manipulations with beneficial or harmful microbes be used to select for sociality like proposed in Figure 2? And vice versa, how does selection on social behaviour (also apart from microbial management) affect interactions with microbes? - Does manipulation of habitat stability select for and against the proposed feedback loop involving sociality and mutualism? - Are there specific ecological factors that consistently facilitate the evolution of insect–microbe mutualisms? - What are the conditions under which our proposed feedback loop does not apply (see Box 2)?

Conflict of interest statement

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10. Batra LR: Insect–Fungus Symbiosis: Nutrition, Mutualism and Commensalism. Allanheld, Osmun; 1979. 11. Vega FE, Blackwell M: Insect–Fungal Associations: Ecology and Evolution. New York: Oxford University Press; 2005. 12. Francke-Grosmann H: Ectosymbiosis in wood-inhabiting beetles. In Symbiosis. Edited by Henry SM. Academic Press; 1967:141-205. 13. Ho¨lldobler B, Wilson EO: The Superorganism: The Beauty, Elegance and Strangeness of Insect Societies. W.W. Norton; 2009. 14. Akcay E: In Evolutionary Models of Mutualism. Edited by Bronstein JL. New York: Oxford Univ Press; 2015.

The authors declare no conflict of interest.

15. Korb J: Towards a more pluralistic view of termite social evolution. Ecol Entomol 2016, 41:34-36.

Acknowledgements

16. Stensmyr MC, Dweck HK, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S et al.: A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 2012, 151:1345-1357.

We acknowledge the invitation of Amy Toth and Adam Dolezal to contribute an article to this special issue. The work of both MR and PHWB Q4 is funded by the German Research Foundation (DFG); MR by grant number RO3523/3-2 and PHWB by Emmy Noether grant number BI1956/ 1-1. PHWB is also supported by a Marie Curie Intra-European Fellowship (IEF) (project number 626279).

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:

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microbes defend their hosts against predators, parasites or pathogens. Most interesting is the discussion about the ecology and evolution of these defensive symbioses.

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Turnbull C, Wilson PD, Hoggard S, Gillings M, Palmer C, Smith S, Beattie D, Hussey S, Stow A, Beattie A: Primordial enemies: fungal pathogens in thrips societies. PLoS ONE 2012, 7:e49737.

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Florez LV, Biedermann PH, Engl T, Kaltenpoth M: Defensive symbioses of animals with prokaryotic and eukaryotic microorganisms. Nat Prod Rep 2015, 32:904-936. In this article the authors comprehensively review the underlying chemistry of all known examples of symbiotic interactions between animals and micrrorganisms, including bacteria, fungi and dinoflagellates, where

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17. Currie CR, Stuart AE: Weeding and grooming of pathogens in agriculture by ants. Proc R Soc Lond Ser B: Biol Sci 2001, 268:1033-1039. 18. Pedrini N, Ortiz-Urquiza A, Huarte-Bonnet C, Fan YH, Juarez P, Keyhani NO: Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen. Proc Natl Acad Sci U S A 2015, 112:E3651-E3660.

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19. Meunier J: Social Immunity and the Evolution of Group Living in Insects. 2015. This excellent review defines social immunity in a broad sense and shows that this socially mediated defense is not only restricted to eusocial insects, but is also present in semisocial or subsocial systems. In contrast to our view the author claims that social immunity evolved as a response to pathogen pressures in social groups and is not considering the possibility that pathogens could also be a driver of social evolution.

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20. Cremer S, Armitage SAO, Schmid-Hempel P: Social immunity. Curr Biol 2007, 17:R693-R702.

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25. Wertheim B, Marchais J, Vet LEM, Dicke M: Allee effect in larval resource exploitation in Drosophila: an interaction among density of adults, larvae, and micro-organisms. Ecol Entomol 2002, 27:608-617. 26. Rohlfs M: Clash of kingdoms or why Drosophila larvae positively respond to fungal competitors. Front Zool 2005, 2:2. 27. Begon M: Yeast and Drosophila. In The Genetics and Biology of Drosophila. Edited by Ashburner M, Carson HL, Thompson JN. Academic Press Inc.; 1982. 28. Stamps JA, Yang LH, Morales VM, Boundy-Mills KL: Drosophila regulate yeast density and increase yeast community similarity in a natural substrate. PLoS ONE 2012, 7. 29. Rohlfs M: Density-dependent insect–mold interactions: effects on fungal growth and spore production. Mycologia 2005, 97:996-1001. 30. Caballero Ortiz S, Trienens M, Rohlfs M: Induced fungal resistance to insect grazing: reciprocal fitness consequences and fungal gene expression in the Drosophila–Aspergillus model system. PLOS ONE 2013, 8:e74951. 31. Fischer CN, Trautman EP, Crawford JM, Stabb EV, Handelsman J, Broderick NA: Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior. eLife 2017, 6:e18855. This article shows how yeast-bacteria interactions change the metabolic profile of Drosophila breeding sites possibly rendering the substrate inhospitable for insect-killing moulds.

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53. Biedermann PHW, Taborsky M: Larval helpers and age polyethism in ambrosia beetles. Proc Natl Acad Sci U S A 2011, 108:17064-17069. 54. French JRJ, Roeper RA: Interactions of ambrosia beetle, Xyleborus dispar (Coleoptera, Scolytidae), with its symbiotic fungus Ambrosiella hartigii (Fungi imperfecti). Can Entomol 1972, 104:1635-1641. 55. Biedermann PHW, Klepzig KD, Taborsky M, Six DL: Abundance and dynamics of filamentous fungi in the complex ambrosia gardens of the primitively eusocial beetle Xyleborinus saxesenii Ratzeburg (Coleoptera: Curculionidae, Scolytinae). FEMS Microbiol Ecol 2013, 83:711-723. 56. Hulcr J, Mann R, Stelinski LL: The scent of a partner: ambrosia beetles are attracted to volatiles from their fungal symbionts. J Chem Ecol 2011, 37:1374-1377. 57. Biedermann PH, Kaltenpoth M: New synthesis: the chemistry of partner choice in insect–microbe mutualisms. J Chem Ecol 2014, 40:99. 58. Cardoza YJ, Vasanthakumar A, Suazo A, Raffa KF: Survey and phylogenetic analysis of culturable microbes in the oral secretions of three bark beetle species. Entomol Exp Appl 2009, 131:138-147.

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59. Aylward FO, Suen G, Biedermann PH, Adams AS, Scott JJ, Malfatti SA, Glavina del Rio T, Tringe SG, Poulsen M, Raffa KF et al.: Convergent bacterial microbiotas in the fungal agricultural systems of insects. MBio 2014, 5:e02077.

42. Suzuki S: Suppression of fungal development on carcasses by the burying beetle Nicrophorus quadripunctatus (Coleoptera: Silphidae). Entomol Sci 2001, 4:403-405.

60. De Fine Licht HH, Biedermann PHW: Patterns of functional enzyme activity in fungus farming ambrosia beetles. Front Zool 2012, 9:13.

43. Vogel H, Shukla SP, Engl T, Weiss B, Fischer R, Steiger S, Heckel DG, Kaltenpoth M, Vilcinskas A: The digestive and defensive basis of carcass utilization by the burying beetle and its microbiota. Nat Commun 2017, 8:15186.

61. Biedermann PH, Klepzig KD, Taborsky M: Fungus cultivation by ambrosia beetles: behavior and laboratory breeding success in three xyleborine species. Environ Entomol 2009, 38:1096-1105.

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39. Buser CC, Newcomb RD, Gaskett AC, Goddard MR: Niche construction initiates the evolution of mutualistic interactions. Ecol Lett 2014, 17:1257-1264. This paper shows experimentally a reciprocal benefit of chemical attraction of Drosophila fruits flies to specific isolates of baker’s yeast Saccharomyces cerevisiae. Association with more attractive yeast isolates resulted in higher fly fecundity, and attractive yeasts were more frequently dispersed by adults.

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47. Kandasamy D, Gershenzon J, Hammerbacher A: Volatile organic compounds emitted by fungal associates of conifer bark beetles and their potential in bark beetle control. J Chem Ecol 2016, 42:952-969.

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46. Kirkendall LR, Biedermann PHW, Jordal BH: Evolution and diversity of bark and ambrosia beetles. In Bark Beetles: Biology and Ecology of Native and Invasive Species. Edited by Vega FE, Hofstetter RW. Academic Press; 2015:85-156. This book chapter is an comprehensive update on the evolution of bark and ambrosia beetle behaviours and ecology, from their feeding preferences, morphology, mating systems, nesting structures and social systems. It shows that this — in evolutionary terms — fairly unstudied weevil lineage offers a fantastic opportunity to tackle fundamental questions in evolutionary biology.

32. Rohlfs M, Kurschner L: Saprophagous insect larvae, Drosophila melanogaster, profit from increased species richness in beneficial microbes. J Appl Entomol 2010, 134:667-671.

37. Chandler JA, Eisen JA, Kopp A: Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts. Appl Environ Microbiol 2012, 78:7327-7336.

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45. Jordal B, Cognato A: Molecular phylogeny of bark and ambrosia beetles reveals multiple origins of fungus farming during periods of global warming. BMC Evol Biol 2012, 12:133.

50. Vega F, Simpkins A, Rodrı´guez-Soto M, Infante F, Biedermann P: Artificial diet sandwich reveals subsocial behaviour in the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae). J Appl Entomol 2016.

36. Anagnostou C, Dorsch M, Rohlfs M: Influence of dietary yeasts on Drosophila melanogaster life-history traits. Entomol Exp Appl 2010, 136:1-11.

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44. Jacobs CGC, Steiger S, Heckel DG, Wielsch N, Vilcinskas A, Vogel H: Sex, offspring and carcass determine antimicrobial peptide expression in the burying beetle. Sci Rep 2016, 6.

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63. Schultz TR, Brady SG: Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci U S A 2008, 105:5435-5440.

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69. Korb J, Heinze J: Major hurdles for the evolution of sociality. Annu Rev Entomol 2016, 61:297-316. In this article the authors sythesize the current concepts in social evolution and show that ecological conditions, for example, competition for resources, as well as kin selection are the most important factors shaping social life in animals. They do not discuss the role of pathogens and microbes in general as an additional ecological factor with important fitness consequences for animals.

65. Fernandez-Marin H, Zimmerman JK, Rehner SA, Wcislo WT: Active use of the metapleural glands by ants in controlling fungal infection. Proc R Soc B: Biol Sci 2006, 273:1689-1695. 66. Hart AG, Ratnieks FL: Task partitioning, division of labour and nest compartmentalisation collectively isolate hazardous waste in the leafcutting ant Atta cephalotes. Behav Ecol Sociobiol 2001, 49:387-392.

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