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Sociality and communicative complexity: insights from the other insect societies
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Sociality and communicative complexity: insights from the other insect societies Volker Nehring1 and Sandra Steiger2 Recognition and communication are essential processes, when it comes to interaction of organisms with their biotic environment. As especially social interactions are coordinated by communication, it has been predicted that social evolution drives communicative complexity. However, studies comparing olfactory signals or receptor repertoires of solitary and eusocial insects found only mixed evidence for the social complexity hypothesis. We present some possible explanations and especially argue that our current knowledge of intermediate levels of sociality is insufficient to fully test the hypothesis, for which a more balanced comparative dataset would be required. We illustrate with chosen examples how complex communication within the other insect societies can be: Many messages are not unique to eusocial insects. Studying the other insect societies will provide us with a more detailed picture of the link between social and communicative complexity. Addresses 1 Department for Evolutionary Biology and Animal Ecology, University of Freiburg, 79104 Freiburg, Germany 2 Institute of Insect Biotechnology, University of Gießen, 35392 Gießen, Germany Corresponding authors: Nehring, Volker ([email protected]), Steiger, Sandra ([email protected])
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Current Opinion in Insect Science 2018, 28:xx–yy
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This review comes from a themed issue on Social insects section
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Edited by Joel Meunier and Sandra Steiger
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https://doi.org/10.1016/j.cois.2018.04.002
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2214-5745/ã 2018 Published by Elsevier Inc.
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Introduction
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The beauty and surprising complexity of animal communication has always fascinated both scientists and laypeople alike. From birdsong to bee dance, interactions between individuals are almost always coordinated by communication [1]. Cooperation in groups, such as mammalian societies or the large colonies of social insects, appears to require the most intricate coordination. Social evolution has therefore been predicted to drive the complexity of recognition and communicative systems and cognitive abilities (‘social complexity hypothesis’,
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Figure 1a) [2–4]. The hypothesis has found support in diverse vertebrate taxa [2,5]. For example in grounddwelling sciurids, species living in more complex social systems produce a higher number of distinct alarm call [6]. However, when it comes to insects, empirical evidence for such a pattern is rather mixed.
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In our review, we shortly introduce insect studies that tested the ‘social complexity hypothesis’ and analyse potential reasons for the lack of a clear support. We highlight that studying communication in The Other Insect Societies can help us fill some of the gaps in order to better understand the relationship between communication and social evolution.
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‘The social complexity hypothesis’: evidence from insect social evolution
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There are currently a few studies available that analysed the relationship between insect social evolution and communicative complexity. In insects, the olfactory channel is the most dominant one and a variety of information is conveyed by pheromones and chemical cues. Consequently, it is not surprising that the majority of the studies focused on chemical communication. The currently best studied group of chemical compounds that play an important role in recognition and communication are cuticular hydrocarbons (CHCs), chemicals that are omnipresent on the cuticular surface of insects [7]. They are known to contain information of, for example, sex, fertility, caste, and kin. Because coordination of groups requires various messages to be exchanged, CHC profiles have been predicted to increase in complexity with the emergence of eusociality (Figure 1a). However, a large comparative study analysing CHC profiles of 241 hymenopteran species found no difference in the number of substance classes and isomers between solitary and eusocial insects [8]. In fact, the polyphyletic group of solitary parasitoid wasps produced some of the most complex CHC profiles across the Hymenoptera, with ants having slightly less complex CHC profiles. Bees and social wasps, however, bear surprisingly simple CHC blends, in particular when considering their social complexity.
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When looking at the receiver side of communication, there is no clear-cut picture either. A study by Zhou et al. [9] compared the chemoreceptor repertoire of 13 solitary and social Hymenoptera and found that the evolution of sociality does not necessarily increase the numbers of, or positive selection on, odorant receptor
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Figure 1
Solitary
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Complexity of the communication system
complexity
(b) Precursor
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Time Current Opinion in Insect Science
Three major hypotheses that predict how communication systems evolve along a gradient of sociality. (a) According to the ‘social complexity hypothesis’, communicative complexity increases with social complexity. (b) The ‘precursor hypothesis’ predicts that the evolution of sociality is more likely to occur in species already equipped with a complex ‘communicative repertoire’. (c) The ‘conflict hypothesis’ predicts that communicative complexity peaks at intermediate level of sociality, where conflict between group members is more likely to occur and where group members are more likely to be recognised individually. The complexity of the communication system is plotted against evolutionary time and the social complexity coded for by colour. The dotted line depicts a solitary species evolving from the same ancestor.
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(OR) genes ([9,see also 10]). In fact, phylogenetic comparisons of multiple solitary and social lineages suggest that a chemoreceptor repertoire expansion may have preceded the evolution of eusociality [9]. Interestingly, the pattern for OR gene and CHC complexity is very similar, with ants having twice as many OR genes than the social bees. Considering that the 9-exon ORs that bind to CHCs are narrowly tuned, with each OR mostly binding to only one or very few substances [11], a simple prediction is that OR and CHC complexity coevolve, with each additional CHC that is used in communication requiring an additional OR. Current Opinion in Insect Science 2018, 28:1–7
Another recent study compared solitary and eusocial halictid bees and used sensilla density on antennae as a proxy for communicative complexity [12]. They found that, while sensilla density is lower in secondary solitary halictid bees than in the eusocial ones, the ancestral state seems to be a solitary bee with high density; again, high sensilla density appears to have preceded the evolution of eusociality. Also studies examining the relationship of sociality and investment in insect mushroom bodies, brain centres that participate in olfactory associative learning, olfactory processing, and sensory integration, did not reveal a clear pattern. A comparative study of wasp brain morphology indicates that sociality has not increased but reduced the investment into the mushroom body [13]. However, other studies have shown that mushroom bodies of social reproductives are larger than those of solitary reproductives in a facultatively eusocial sweat bee [14], and that mushroom body development is driven by social interactions in ants [15].
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What is a complex communication system?
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A major challenge in testing the ‘social complexity hypothesis’ is to find an accurate measurement of communicative complexity. A number of traits have been used as proxies of complexity in communication systems. However, some traits such as the number of sensilla or the size of brains are not necessarily increasing the quantity of information that is communicated, but rather the quality: sensitivity, precision, and speed of information processing [16]. The large antennae of male moths, for example, have evolved to achieve a stunning sensitivity to the typically not very complex female sex pheromone, whose single message is ‘I am here’ [17,18]. In the same vein, larger numbers of CHCs on an insect’s cuticle and a larger number of OR genes might not necessarily have evolved to communicate a larger number of messages either. In a recognition context, more CHCs and OR genes may simply allow for a more reliable discrimination between individuals through a larger number of possible different odour blend configurations, without increasing the number of messages. This could be important when individuals need to discriminate between many different individuals or multiple different groups of individuals [19].
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As good physiological and morphological proxies for communicative complexity are difficult to find, we suggest ultimate analyses of the interaction between communication and social evolution to focus on the actual messages that are sent, which requires comprehensive ethological studies.
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Lack of data for hypothesis testing and the benefits of studying the other insect societies
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Another major problem that we currently face in testing the social complexity hypothesis is our limited knowledge of communication in insects in general. In most cases, except some well-studied models (honeybee,
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burying beetle), we have no comprehensive overview over the messages that are communicated within a species. Insects often do not only rely on one but different signalling channels, from olfactory to visual and acoustic communication [20]. Analysing all signals that are produced is thus a demanding task, especially when considering that the most dominant signalling channel in insects, the olfactory one, is technically challenging to analyse [17]. The chemical identity of queen pheromones remained unknown for the overwhelming majority of eusocial species for a long time, and even though some progress has been made in the meantime (e.g. [21]), we still only know the molecules involved for a few species. A particular problem is also the disbalance across taxa and degrees of sociality. In general, it is often neglected that primitive aggregations or small family groups, consisting of parents and offspring, are already characterised by relatively complex communication processes [22]. The step from the other social insects or even solitary insects to highly eusocial ones is not necessarily as steep as one might think. To support this point, we present some examples of olfactory communication that are typically attributed to eusocial insects, but can also be found in the other insect societies. However, while these examples are impressive, they are for the most part anecdotal in that we do not know how common the different types of communication are across species. A more comprehensive dataset of communication in the other insect societies would greatly advance our understanding of the role of communication in social evolution.
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Aggregation pheromones
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The highly eusocial honeybees use aggregation pheromones from the mandibular gland to coordinate swarming. Interestingly, the queen mandibular gland pheromone has been co-opted: queens also use it to attract males, attract workers to form the queen retinue, and to keep workers from reproduction [although other substances are involved as well [23]]. Whenever pheromones are co-opted for multiple messages, the machinery for sending and receiving of messages will actually become simpler, which supports the idea that highly eusocial insects need not be the pinnacle when it comes to the complexity of communication systems.
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Even without elaborate interactions between group members, aggregations can increase individual fitness in comparison to a purely solitary life (Allee effects). For instance, group living generally reduces individual predation risk (selfish herd) and can protect from desiccation [18]. As a more specific example, bark beetles can often not overcome tree defences individually and depend on a species-specific set of volatile compounds to attract conspecifics, so that they can attack living or dying trees in large groups and then use them as a resource for reproduction [24]. www.sciencedirect.com
Since Allee effects are very simple and require no elaborate interactions among individuals, aggregation pheromones, which attract conspecifics independent of sex, are phylogenetically very basal and found in species as diverse as bed bugs [25], schooling shrimps [26], nematodes [27], and even amoebozoans that aggregate through chemotaxis to cAMP [28].
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Alarm pheromones
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Alarm pheromones are among the most common pheromones of insects [29]. In large eusocial colonies, individuals under attack can produce volatile alarm pheromones that recruit others for help. The cues are evolutionary derived from substances leaking from wounded bodies [30], or are defence substances used to repel attacking predators. The formic acid that ant workers spray to defend themselves, for example, also recruits their nestmates to help with defence [31]. In smaller and perhaps more ephemeral societies (e.g. in leaf litter), however, alarm pheromones cause colonies do disperse to avoid the threat (‘panic alarms’ [32]). This behaviour would be adaptive for gregarious insects as well.
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Aphids feeding on leaves produce farnesenes upon threat, which cause conspecifics and sometimes even individuals of other species to move away or drop off leaves [29]. Alarm pheromones are further known from thrips [33], collembolans [30], bed bugs [34], and other arthropods, such as mites [35].
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Because alarm pheromones have a highly functional evolutionary origin, and have benefits that can be realised independent of complex social structures, even in loose non-kin groups, there is no reason to expect alarm signalling to be specific to eusocial insects. If anything, the behavioural responses to the pheromones may be rewired to cause a more complex, context-based response.
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Fertility signals
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In eusocial insects, the reproductive division of labour between queens and workers is often maintained by means of pheromones that honestly reflect the reproductive state. Although those queen pheromones can belong to different chemical classes, studies indicate that CHCs often play a key role [21,36]. Recent theoretical considerations suggest a transition of reproductive communication from cue-like signature mixtures, to learned fertility signals, to innate queen pheromones that evolved across eusocial insects [37]. Consequently, according to this hypothesis a chemical repertoire reflecting reproductive state was already available early on, for example to be used for mate choice. In fact, there are also subsocial and even many solitary species in which CHCs co-vary with reproductive state, and queen pheromones might have derived from sex pheromones [36]. In burying beetles, which raise their young on vertebrate cadavers and
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provide elaborate pre-hatching and post-hatching care, CHC profiles of males and females have been shown to change when the beetles are breeding [38]. The information is used by the adults to recognise a breeding partner and discriminate against infanticidal intruders to the brood chamber [39]. How receivers respond to the CHCs certainly differs from eusocial insects: breeder CHCs do not suppress female reproduction. Nevertheless, it exemplifies that information about reproductive state is available and used in subsocial species. Interestingly, during the intensive period of parental care, female burying beetles are known to emit a volatile, methyl geranate, which reliably reflects their temporary infertility during this time [40]. The pheromone has been shown to suppress sexual activity of male partners. An infertility or sterility pheromone has also been reported in worker bumblebees [41]. Here, workers appear to signal to the queen and other workers that they will refrain from producing any eggs, which reduces aggression. Again, the examples highlight that fertility or infertility cues and signals are not specific to eusocial insects; only the type of receiver and its behavioural response deviate depending on the form of interaction and structure of the group.
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Solicitation pheromones
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We know from some eusocial insects that larvae produce chemical substances to solicit food from nurses. In honey bees Apis mellifera, young and old larvae emit pheromones that differ in composition and regulate how much food nurses provide, to meet the nutritional requirements of the larvae [42,43]. Young larvae emit the volatile (E)b-ocimene, whereas older larvae predominantly produce a so-called brood ester pheromone, a blend of 10 ethyl and methyl fatty acid esters. However, such solicitation pheromones are not unique to eusocial groups, but also present in some subsocial insects. In fact, theory predicts the existence of begging signals for all brood caring organisms, where parent and offspring (or helpers and brood) interact and offspring rely on specific resources provided by the parents [44,45]. In the burrower bug, Sehirus cinctus, for example, nymphs release a blend of monoterpenes, which regulates maternal provisioning. Mothers exposed to volatiles from nymphs in poor condition provide significantly more food than those exposed to volatiles from well-fed nymphs [46]. In the European earwig Forficula auricularia CHCs signal the nymph’s nutritional state. However, earwig mothers preferentially feed well-fed nymphs [47].
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Nestmate recognition/kin recognition/individual recognition
Cooperation can only be successful when altruism either benefits relatives or is reciprocated by the receivers. For both interactions to be reliable, some sort of recognition system is necessary to recognise individuals that ‘deserve’ altruism. Eusocial insect workers are selected to direct Current Opinion in Insect Science 2018, 28:1–7
work efforts towards their closest relatives. However, they rarely recognise kinship itself, but simply treat all colony members as kin. This can be demonstrated by transferring young workers, who typically lack nestmate recognition cues, to other colonies, where they blend in and treat their new unrelated nestmates as kin (reviewed in [48]). Individual odours are both genetically and ecologically determined, but cue mixing within the colony leads to a uniform odour that is well delineated against the odours of other colonies [49]. Only few cases of imperfect cue blending are documented, in which genetic lineages within the same colony can in theory be identified based on their odour [50–52]. Evidence that workers are actually able to distinguish genetic lineages (kin recognition) and behave nepotistically is rare. It comes from primitively eusocial ants and paper wasps [53,54] rather than highly eusocial insects. Interestingly, nestmate recognition is lost in some of the largest eusocial insects known: Unicolonial ants with their supercolonies often abandoned nestmate recognition altogether [55].
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Kin recognition has also been demonstrated to facilitate kin-directed cooperation in groups of juveniles in solitary or gregarious arthropods: When groups consist of relatives and non-relatives and resources are scarce, non-relatives are preferentially cannibalised in mites and earwigs [56,57]. Subsocial spiders prefer to reside with cuticular extracts of kin rather than non-kin [58]. In the mite case, it has been documented that kin recognition is learned and not based on hard-wired recognition templates, which might suggest that nestmate recognition and kin recognition rely on similar proxy mechanisms. The odours used for kin recognition are likely to be the same than those used in nestmate recognition: blends of CHCs, which will then be perceived by similar sets of olfactory receptors both in solitary and social insects.
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A different context for kin recognition is mate choice: Information about kinship can prevent inbreeding, and it is known that cockroaches [59] and solitary parasitoid waps [60] use CHCs to preferentially mate with non-kin. There may be cases in which the processes differ from those discussed above, for example when volatile sex pheromones are involved (for example in the beewolf [61]), or in case templates for mate choice are genetically determined rather than learned.
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Evidence for individual recognition in insects is very rare. It is difficult to prove because it is often confounded with group-level recognition [62]. However, we know that ant queens in primitive Pachycondyla societies use odours to recognise each other individually, which supports the stability of dominance hierarchies ([63,there is a similar case but with visual cues in paper wasps, 64]). Interestingly, this ability is only predicted for these primitive societies and absent from large eusocial insect colonies [65].
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The overall pattern is thus that some sort of kin recognition is common for all levels of social complexity, with perhaps the highest information content at intermediate levels: In small societies of primitively eusocial species, where dominance is established through individual interactions and conflict over reproduction is high, group-level, kin-level, and individual recognition are all employed simultaneously.
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Recruitment/trail pheromones
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Trail pheromones are only expected to evolve in cooperative groups where individuals forage for patchy resources on foot: they evolved more than once in ants and are well studied in termites as well [20]. Flying eusocial insects can use volatiles to attract nestmates to food sources (e.g. Nasanov pheromone in honeybees [23]). Trail pheromones are also known from group-living non-eusocial insects such as tent caterpillars [18]. In eusocial or subsocial groups that do not forage but live in their food, such as on-piece nesting termites or burying beetles, trails are not expected. However, we know that parasites do eavesdrop on trail pheromones and it has been speculated that trail pheromones evolved from individuals eavesdropping on the footprints or faeces of their competitors inevitably deposit [66–68], in which case the receiver systems for trail following might have been already in place before the evolution of sociality.
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Alternative hypotheses
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Although the ‘social complexity hypothesis’ sounds intuitive, we have to emphasise that also alternative hypotheses on the link between sociality and communication have been suggested. Comprehensively studying intermediate levels of sociality in the Other Insect Societies will allow us to differentiate between the social complexity hypothesis and two alternatives that have been put forward. Instead of sociality being a driver of communicative complexity, a complex or very sensitive and accurate communication system may be a necessary precursor that allows social evolution to occur (‘precursor hypothesis’, Figure 1b [8]). The evolution of individual or group-level recognition, a necessity for stable groups, might only be possible after other evolutionary forces caused CHC profiles to become complex enough to allow for reliable recognition. This would also be in line with the current picture that within the hymenoptera there was an OR gene family expansion prior to the evolution of sociality [9]. However, as Zhou et al. point out, we currently do not have reliable OR gene annotations for enough species to conduct a formal phylogenetically balanced analysis of this question.
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A second alternative hypothesis is that the investment in recognition processes and brains may peak at intermediate levels of sociality and decrease in highly eusocial insects (‘conflict hypothesis’, Figure 1c) [13,69]. In many primitively eusocial species, reproductive monopoly is www.sciencedirect.com
only maintained through dominance hierarchies, the maintenance of which relies on individual recognition or at least on the ability to judge the reproductive state of others. This conflict causes particular selection on receivers to pick up any fertility or other cues that might give away cheaters. In brood-caring species, such as the biparental burying beetles, conflicts between the sexes, siblings, and parents and offspring are omnipresent and may have driven the evolution of rather sophisticated recognition and communication processes [70]. This contrasts with obligate eusocial insects and their permanent reproductive division of labour between queen and sterile worker castes, where conflict over direct reproduction is low [71]. In line with the social conflict hypothesis, primitive societies are often based on the capacity to recognise both individuals and group members [13,72]. Highly eusocial insects, in contrast, rely on class-level recognition, which is a less sophisticated recognition process than for example individual recognition [19].
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Conclusions
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The hypothesis that the complexity of communication systems is driven by the evolution of complex social systems is an intuitive one but so far lacks evidence in insects. We suggest that we currently do not have the data that would be necessary to unveil the true connection between social and communicative complexity. So far, our best shot are comparative studies of facultatively social species or taxonomically narrow groups with well-documented life histories and communication systems (e.g. [12,14]). Broad comparative studies are bound to fail because sociality is not a binary variable but a continuum on which we cannot properly place most of the species due to missing data. Communicative complexity is likely to vary gradually along this continuum, with sometimes surprisingly high complexity in the other insect societies. Social evolution should influence the quantity and quality of messages that are communicated, which has been exhaustively analysed only for very few species. The current sample is highly biased towards eusocial Hymenoptera.
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With this short review we would like to emphasise that studying the other social insects will help us to better understand the evolutionary connection between social and communicative complexity. That way we will fill in the blanks on the sociality continuum and generate valuable phylogenetically independent data points for the lower and intermediate levels of complexity.
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Conflict of interest statement
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Nothing declared.
Acknowledgements
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472 We thank Joel Meunier and an anonymous reviewer for helpful comments and we acknowledge funding provided by the German Research Q3473 474 Foundation (DFG) to SS (STE 1874/3-3 and STE 1874/7-1).
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Sociality and communicative complexity: insights from the other insect societies Volker Nehring1 and Sandra Steiger2 Recognition and communication are essential processes, when it comes to interaction of organisms with their biotic environment. As especially social interactions are coordinated by communication, it has been predicted that social evolution drives communicative complexity. However, studies comparing olfactory signals or receptor repertoires of solitary and eusocial insects found only mixed evidence for the social complexity hypothesis. We present some possible explanations and especially argue that our current knowledge of intermediate levels of sociality is insufficient to fully test the hypothesis, for which a more balanced comparative dataset would be required. We illustrate with chosen examples how complex communication within the other insect societies can be: Many messages are not unique to eusocial insects. Studying the other insect societies will provide us with a more detailed picture of the link between social and communicative complexity. Addresses 1 Department for Evolutionary Biology and Animal Ecology, University of Freiburg, 79104 Freiburg, Germany 2 Institute of Insect Biotechnology, University of Gießen, 35392 Gießen, Germany Corresponding authors: Nehring, Volker ([email protected]), Steiger, Sandra ([email protected])
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This review comes from a themed issue on Social insects section
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https://doi.org/10.1016/j.cois.2018.04.002
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2214-5745/ã 2018 Published by Elsevier Inc.
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Introduction
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The beauty and surprising complexity of animal communication has always fascinated both scientists and laypeople alike. From birdsong to bee dance, interactions between individuals are almost always coordinated by communication [1]. Cooperation in groups, such as mammalian societies or the large colonies of social insects, appears to require the most intricate coordination. Social evolution has therefore been predicted to drive the complexity of recognition and communicative systems and cognitive abilities (‘social complexity hypothesis’,
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Figure 1a) [2–4]. The hypothesis has found support in diverse vertebrate taxa [2,5]. For example in grounddwelling sciurids, species living in more complex social systems produce a higher number of distinct alarm call [6]. However, when it comes to insects, empirical evidence for such a pattern is rather mixed.
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In our review, we shortly introduce insect studies that tested the ‘social complexity hypothesis’ and analyse potential reasons for the lack of a clear support. We highlight that studying communication in The Other Insect Societies can help us fill some of the gaps in order to better understand the relationship between communication and social evolution.
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‘The social complexity hypothesis’: evidence from insect social evolution
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There are currently a few studies available that analysed the relationship between insect social evolution and communicative complexity. In insects, the olfactory channel is the most dominant one and a variety of information is conveyed by pheromones and chemical cues. Consequently, it is not surprising that the majority of the studies focused on chemical communication. The currently best studied group of chemical compounds that play an important role in recognition and communication are cuticular hydrocarbons (CHCs), chemicals that are omnipresent on the cuticular surface of insects [7]. They are known to contain information of, for example, sex, fertility, caste, and kin. Because coordination of groups requires various messages to be exchanged, CHC profiles have been predicted to increase in complexity with the emergence of eusociality (Figure 1a). However, a large comparative study analysing CHC profiles of 241 hymenopteran species found no difference in the number of substance classes and isomers between solitary and eusocial insects [8]. In fact, the polyphyletic group of solitary parasitoid wasps produced some of the most complex CHC profiles across the Hymenoptera, with ants having slightly less complex CHC profiles. Bees and social wasps, however, bear surprisingly simple CHC blends, in particular when considering their social complexity.
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When looking at the receiver side of communication, there is no clear-cut picture either. A study by Zhou et al. [9] compared the chemoreceptor repertoire of 13 solitary and social Hymenoptera and found that the evolution of sociality does not necessarily increase the numbers of, or positive selection on, odorant receptor
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Figure 1
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Three major hypotheses that predict how communication systems evolve along a gradient of sociality. (a) According to the ‘social complexity hypothesis’, communicative complexity increases with social complexity. (b) The ‘precursor hypothesis’ predicts that the evolution of sociality is more likely to occur in species already equipped with a complex ‘communicative repertoire’. (c) The ‘conflict hypothesis’ predicts that communicative complexity peaks at intermediate level of sociality, where conflict between group members is more likely to occur and where group members are more likely to be recognised individually. The complexity of the communication system is plotted against evolutionary time and the social complexity coded for by colour. The dotted line depicts a solitary species evolving from the same ancestor.
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(OR) genes ([9,see also 10]). In fact, phylogenetic comparisons of multiple solitary and social lineages suggest that a chemoreceptor repertoire expansion may have preceded the evolution of eusociality [9]. Interestingly, the pattern for OR gene and CHC complexity is very similar, with ants having twice as many OR genes than the social bees. Considering that the 9-exon ORs that bind to CHCs are narrowly tuned, with each OR mostly binding to only one or very few substances [11], a simple prediction is that OR and CHC complexity coevolve, with each additional CHC that is used in communication requiring an additional OR. Current Opinion in Insect Science 2018, 28:1–7
Another recent study compared solitary and eusocial halictid bees and used sensilla density on antennae as a proxy for communicative complexity [12]. They found that, while sensilla density is lower in secondary solitary halictid bees than in the eusocial ones, the ancestral state seems to be a solitary bee with high density; again, high sensilla density appears to have preceded the evolution of eusociality. Also studies examining the relationship of sociality and investment in insect mushroom bodies, brain centres that participate in olfactory associative learning, olfactory processing, and sensory integration, did not reveal a clear pattern. A comparative study of wasp brain morphology indicates that sociality has not increased but reduced the investment into the mushroom body [13]. However, other studies have shown that mushroom bodies of social reproductives are larger than those of solitary reproductives in a facultatively eusocial sweat bee [14], and that mushroom body development is driven by social interactions in ants [15].
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What is a complex communication system?
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A major challenge in testing the ‘social complexity hypothesis’ is to find an accurate measurement of communicative complexity. A number of traits have been used as proxies of complexity in communication systems. However, some traits such as the number of sensilla or the size of brains are not necessarily increasing the quantity of information that is communicated, but rather the quality: sensitivity, precision, and speed of information processing [16]. The large antennae of male moths, for example, have evolved to achieve a stunning sensitivity to the typically not very complex female sex pheromone, whose single message is ‘I am here’ [17,18]. In the same vein, larger numbers of CHCs on an insect’s cuticle and a larger number of OR genes might not necessarily have evolved to communicate a larger number of messages either. In a recognition context, more CHCs and OR genes may simply allow for a more reliable discrimination between individuals through a larger number of possible different odour blend configurations, without increasing the number of messages. This could be important when individuals need to discriminate between many different individuals or multiple different groups of individuals [19].
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As good physiological and morphological proxies for communicative complexity are difficult to find, we suggest ultimate analyses of the interaction between communication and social evolution to focus on the actual messages that are sent, which requires comprehensive ethological studies.
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Lack of data for hypothesis testing and the benefits of studying the other insect societies
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Another major problem that we currently face in testing the social complexity hypothesis is our limited knowledge of communication in insects in general. In most cases, except some well-studied models (honeybee,
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burying beetle), we have no comprehensive overview over the messages that are communicated within a species. Insects often do not only rely on one but different signalling channels, from olfactory to visual and acoustic communication [20]. Analysing all signals that are produced is thus a demanding task, especially when considering that the most dominant signalling channel in insects, the olfactory one, is technically challenging to analyse [17]. The chemical identity of queen pheromones remained unknown for the overwhelming majority of eusocial species for a long time, and even though some progress has been made in the meantime (e.g. [21]), we still only know the molecules involved for a few species. A particular problem is also the disbalance across taxa and degrees of sociality. In general, it is often neglected that primitive aggregations or small family groups, consisting of parents and offspring, are already characterised by relatively complex communication processes [22]. The step from the other social insects or even solitary insects to highly eusocial ones is not necessarily as steep as one might think. To support this point, we present some examples of olfactory communication that are typically attributed to eusocial insects, but can also be found in the other insect societies. However, while these examples are impressive, they are for the most part anecdotal in that we do not know how common the different types of communication are across species. A more comprehensive dataset of communication in the other insect societies would greatly advance our understanding of the role of communication in social evolution.
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Aggregation pheromones
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The highly eusocial honeybees use aggregation pheromones from the mandibular gland to coordinate swarming. Interestingly, the queen mandibular gland pheromone has been co-opted: queens also use it to attract males, attract workers to form the queen retinue, and to keep workers from reproduction [although other substances are involved as well [23]]. Whenever pheromones are co-opted for multiple messages, the machinery for sending and receiving of messages will actually become simpler, which supports the idea that highly eusocial insects need not be the pinnacle when it comes to the complexity of communication systems.
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Even without elaborate interactions between group members, aggregations can increase individual fitness in comparison to a purely solitary life (Allee effects). For instance, group living generally reduces individual predation risk (selfish herd) and can protect from desiccation [18]. As a more specific example, bark beetles can often not overcome tree defences individually and depend on a species-specific set of volatile compounds to attract conspecifics, so that they can attack living or dying trees in large groups and then use them as a resource for reproduction [24]. www.sciencedirect.com
Since Allee effects are very simple and require no elaborate interactions among individuals, aggregation pheromones, which attract conspecifics independent of sex, are phylogenetically very basal and found in species as diverse as bed bugs [25], schooling shrimps [26], nematodes [27], and even amoebozoans that aggregate through chemotaxis to cAMP [28].
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Alarm pheromones
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Alarm pheromones are among the most common pheromones of insects [29]. In large eusocial colonies, individuals under attack can produce volatile alarm pheromones that recruit others for help. The cues are evolutionary derived from substances leaking from wounded bodies [30], or are defence substances used to repel attacking predators. The formic acid that ant workers spray to defend themselves, for example, also recruits their nestmates to help with defence [31]. In smaller and perhaps more ephemeral societies (e.g. in leaf litter), however, alarm pheromones cause colonies do disperse to avoid the threat (‘panic alarms’ [32]). This behaviour would be adaptive for gregarious insects as well.
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Aphids feeding on leaves produce farnesenes upon threat, which cause conspecifics and sometimes even individuals of other species to move away or drop off leaves [29]. Alarm pheromones are further known from thrips [33], collembolans [30], bed bugs [34], and other arthropods, such as mites [35].
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Because alarm pheromones have a highly functional evolutionary origin, and have benefits that can be realised independent of complex social structures, even in loose non-kin groups, there is no reason to expect alarm signalling to be specific to eusocial insects. If anything, the behavioural responses to the pheromones may be rewired to cause a more complex, context-based response.
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Fertility signals
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In eusocial insects, the reproductive division of labour between queens and workers is often maintained by means of pheromones that honestly reflect the reproductive state. Although those queen pheromones can belong to different chemical classes, studies indicate that CHCs often play a key role [21,36]. Recent theoretical considerations suggest a transition of reproductive communication from cue-like signature mixtures, to learned fertility signals, to innate queen pheromones that evolved across eusocial insects [37]. Consequently, according to this hypothesis a chemical repertoire reflecting reproductive state was already available early on, for example to be used for mate choice. In fact, there are also subsocial and even many solitary species in which CHCs co-vary with reproductive state, and queen pheromones might have derived from sex pheromones [36]. In burying beetles, which raise their young on vertebrate cadavers and
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provide elaborate pre-hatching and post-hatching care, CHC profiles of males and females have been shown to change when the beetles are breeding [38]. The information is used by the adults to recognise a breeding partner and discriminate against infanticidal intruders to the brood chamber [39]. How receivers respond to the CHCs certainly differs from eusocial insects: breeder CHCs do not suppress female reproduction. Nevertheless, it exemplifies that information about reproductive state is available and used in subsocial species. Interestingly, during the intensive period of parental care, female burying beetles are known to emit a volatile, methyl geranate, which reliably reflects their temporary infertility during this time [40]. The pheromone has been shown to suppress sexual activity of male partners. An infertility or sterility pheromone has also been reported in worker bumblebees [41]. Here, workers appear to signal to the queen and other workers that they will refrain from producing any eggs, which reduces aggression. Again, the examples highlight that fertility or infertility cues and signals are not specific to eusocial insects; only the type of receiver and its behavioural response deviate depending on the form of interaction and structure of the group.
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Solicitation pheromones
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We know from some eusocial insects that larvae produce chemical substances to solicit food from nurses. In honey bees Apis mellifera, young and old larvae emit pheromones that differ in composition and regulate how much food nurses provide, to meet the nutritional requirements of the larvae [42,43]. Young larvae emit the volatile (E)b-ocimene, whereas older larvae predominantly produce a so-called brood ester pheromone, a blend of 10 ethyl and methyl fatty acid esters. However, such solicitation pheromones are not unique to eusocial groups, but also present in some subsocial insects. In fact, theory predicts the existence of begging signals for all brood caring organisms, where parent and offspring (or helpers and brood) interact and offspring rely on specific resources provided by the parents [44,45]. In the burrower bug, Sehirus cinctus, for example, nymphs release a blend of monoterpenes, which regulates maternal provisioning. Mothers exposed to volatiles from nymphs in poor condition provide significantly more food than those exposed to volatiles from well-fed nymphs [46]. In the European earwig Forficula auricularia CHCs signal the nymph’s nutritional state. However, earwig mothers preferentially feed well-fed nymphs [47].
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Cooperation can only be successful when altruism either benefits relatives or is reciprocated by the receivers. For both interactions to be reliable, some sort of recognition system is necessary to recognise individuals that ‘deserve’ altruism. Eusocial insect workers are selected to direct Current Opinion in Insect Science 2018, 28:1–7
work efforts towards their closest relatives. However, they rarely recognise kinship itself, but simply treat all colony members as kin. This can be demonstrated by transferring young workers, who typically lack nestmate recognition cues, to other colonies, where they blend in and treat their new unrelated nestmates as kin (reviewed in [48]). Individual odours are both genetically and ecologically determined, but cue mixing within the colony leads to a uniform odour that is well delineated against the odours of other colonies [49]. Only few cases of imperfect cue blending are documented, in which genetic lineages within the same colony can in theory be identified based on their odour [50–52]. Evidence that workers are actually able to distinguish genetic lineages (kin recognition) and behave nepotistically is rare. It comes from primitively eusocial ants and paper wasps [53,54] rather than highly eusocial insects. Interestingly, nestmate recognition is lost in some of the largest eusocial insects known: Unicolonial ants with their supercolonies often abandoned nestmate recognition altogether [55].
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Kin recognition has also been demonstrated to facilitate kin-directed cooperation in groups of juveniles in solitary or gregarious arthropods: When groups consist of relatives and non-relatives and resources are scarce, non-relatives are preferentially cannibalised in mites and earwigs [56,57]. Subsocial spiders prefer to reside with cuticular extracts of kin rather than non-kin [58]. In the mite case, it has been documented that kin recognition is learned and not based on hard-wired recognition templates, which might suggest that nestmate recognition and kin recognition rely on similar proxy mechanisms. The odours used for kin recognition are likely to be the same than those used in nestmate recognition: blends of CHCs, which will then be perceived by similar sets of olfactory receptors both in solitary and social insects.
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A different context for kin recognition is mate choice: Information about kinship can prevent inbreeding, and it is known that cockroaches [59] and solitary parasitoid waps [60] use CHCs to preferentially mate with non-kin. There may be cases in which the processes differ from those discussed above, for example when volatile sex pheromones are involved (for example in the beewolf [61]), or in case templates for mate choice are genetically determined rather than learned.
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Evidence for individual recognition in insects is very rare. It is difficult to prove because it is often confounded with group-level recognition [62]. However, we know that ant queens in primitive Pachycondyla societies use odours to recognise each other individually, which supports the stability of dominance hierarchies ([63,there is a similar case but with visual cues in paper wasps, 64]). Interestingly, this ability is only predicted for these primitive societies and absent from large eusocial insect colonies [65].
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The overall pattern is thus that some sort of kin recognition is common for all levels of social complexity, with perhaps the highest information content at intermediate levels: In small societies of primitively eusocial species, where dominance is established through individual interactions and conflict over reproduction is high, group-level, kin-level, and individual recognition are all employed simultaneously.
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Trail pheromones are only expected to evolve in cooperative groups where individuals forage for patchy resources on foot: they evolved more than once in ants and are well studied in termites as well [20]. Flying eusocial insects can use volatiles to attract nestmates to food sources (e.g. Nasanov pheromone in honeybees [23]). Trail pheromones are also known from group-living non-eusocial insects such as tent caterpillars [18]. In eusocial or subsocial groups that do not forage but live in their food, such as on-piece nesting termites or burying beetles, trails are not expected. However, we know that parasites do eavesdrop on trail pheromones and it has been speculated that trail pheromones evolved from individuals eavesdropping on the footprints or faeces of their competitors inevitably deposit [66–68], in which case the receiver systems for trail following might have been already in place before the evolution of sociality.
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Alternative hypotheses
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Although the ‘social complexity hypothesis’ sounds intuitive, we have to emphasise that also alternative hypotheses on the link between sociality and communication have been suggested. Comprehensively studying intermediate levels of sociality in the Other Insect Societies will allow us to differentiate between the social complexity hypothesis and two alternatives that have been put forward. Instead of sociality being a driver of communicative complexity, a complex or very sensitive and accurate communication system may be a necessary precursor that allows social evolution to occur (‘precursor hypothesis’, Figure 1b [8]). The evolution of individual or group-level recognition, a necessity for stable groups, might only be possible after other evolutionary forces caused CHC profiles to become complex enough to allow for reliable recognition. This would also be in line with the current picture that within the hymenoptera there was an OR gene family expansion prior to the evolution of sociality [9]. However, as Zhou et al. point out, we currently do not have reliable OR gene annotations for enough species to conduct a formal phylogenetically balanced analysis of this question.
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A second alternative hypothesis is that the investment in recognition processes and brains may peak at intermediate levels of sociality and decrease in highly eusocial insects (‘conflict hypothesis’, Figure 1c) [13,69]. In many primitively eusocial species, reproductive monopoly is www.sciencedirect.com
only maintained through dominance hierarchies, the maintenance of which relies on individual recognition or at least on the ability to judge the reproductive state of others. This conflict causes particular selection on receivers to pick up any fertility or other cues that might give away cheaters. In brood-caring species, such as the biparental burying beetles, conflicts between the sexes, siblings, and parents and offspring are omnipresent and may have driven the evolution of rather sophisticated recognition and communication processes [70]. This contrasts with obligate eusocial insects and their permanent reproductive division of labour between queen and sterile worker castes, where conflict over direct reproduction is low [71]. In line with the social conflict hypothesis, primitive societies are often based on the capacity to recognise both individuals and group members [13,72]. Highly eusocial insects, in contrast, rely on class-level recognition, which is a less sophisticated recognition process than for example individual recognition [19].
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Conclusions
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The hypothesis that the complexity of communication systems is driven by the evolution of complex social systems is an intuitive one but so far lacks evidence in insects. We suggest that we currently do not have the data that would be necessary to unveil the true connection between social and communicative complexity. So far, our best shot are comparative studies of facultatively social species or taxonomically narrow groups with well-documented life histories and communication systems (e.g. [12,14]). Broad comparative studies are bound to fail because sociality is not a binary variable but a continuum on which we cannot properly place most of the species due to missing data. Communicative complexity is likely to vary gradually along this continuum, with sometimes surprisingly high complexity in the other insect societies. Social evolution should influence the quantity and quality of messages that are communicated, which has been exhaustively analysed only for very few species. The current sample is highly biased towards eusocial Hymenoptera.
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With this short review we would like to emphasise that studying the other social insects will help us to better understand the evolutionary connection between social and communicative complexity. That way we will fill in the blanks on the sociality continuum and generate valuable phylogenetically independent data points for the lower and intermediate levels of complexity.
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Conflict of interest statement
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Nothing declared.
Acknowledgements
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472 We thank Joel Meunier and an anonymous reviewer for helpful comments and we acknowledge funding provided by the German Research Q3473 474 Foundation (DFG) to SS (STE 1874/3-3 and STE 1874/7-1).
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Please cite this article in press as: Nehring V, Steiger S: Sociality and communicative complexity: insights from the other insect societies, Curr Opin Insect Sci (2018), https://doi.org/10.1016/j. cois.2018.04.002