Inter-caste communication in social insects

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Highlights

  • We review advances in our understanding of communication between males and females, queens and worker castes.

  • Calcium imaging or genomics start to reveal how pheromones are processed in the nervous system.

Social insect colonies function as highly integrated units despite consisting of many individuals. This requires the different functional parts of the colony (e.g. different castes) to exchange information that aid in colony functioning and ontogeny. Here we discuss inter-caste communication in three contexts, firstly, the communication between males and females during courtship, secondly, the communication between queens and workers that regulate reproduction and thirdly, the communication between worker castes that allows colonies to balance the number of different worker types. Some signals show surprising complexity in both their chemistry and function, whereas others are simple compounds that were probably already used as pheromones in the solitary ancestors of several social insect lineages.

Introduction

Insect colonies often consist of thousands  and sometimes millions  of individuals and the success of individuals depends crucially on the success of the colony [1, 2]. Colonies show two kinds of division of labor. First, there is a reproductive division of labor between queens (and kings in termites) and the largely sterile workers. Second, there is division of labor among the workers for tasks like brood rearing, colony defense or foraging [1, 2]. Communication between and within the different castes (queens, males and different worker groups) is fundamental for the efficient functioning of a colony. In order for colonies to respond to the often changing needs, workers  like the cells of multicellular organisms  need to respond to signals in ways that are beneficial to the whole complex system.

Most communication is based on chemical signals (or pheromones) that are produced by exocrine glands [1, 2, 3, 4]. Hundreds of chemicals produced in more than 60 different glands have been identified in social insects [3, 5], which has led researchers to refer to social insects as chemical factories [1]. Traditionally, pheromones have been divided into two classes, primer and releaser pheromones [1]. A releaser pheromone initiates an immediate behavioral response, whereas a primer pheromone alters more long-term endocrine and reproductive systems in the recipient [6]. However, it has become clear that there are pheromones that have both releaser and primer effects [6, 7, 8]. The pheromone signals are perceived via olfactory sensillae on the antennae [3, 9, 10•, 11•] before being further processed by the olfactory system [12].

In this review we focus on recent advances in our understanding of inter-caste communication in three important contexts: firstly, communication between male and female reproductives that results in mating and, subsequently, colony foundation, secondly, communication between queens and workers to regulate reproduction and thirdly, communication between different functional groups of workers (sometimes called sub-castes) that allows colonies to balance the number of workers performing different tasks (for communication within castes, for example, among foragers during resource collection or during house hunting see [13, 14, 15, 16]). Recent research has highlighted the importance of chemical and behavioral complexity, context, and dose for communication [6]. Furthermore, the recent identification of several queen signals that inhibit reproduction in workers [7, 17••, 18] or other queens [19] has improved our understanding of the evolution of reproductive division of labor. New tools like calcium imaging or genomics have started to reveal how pheromone signals are processed in the nervous system [12, 20] and how external cues and signals induce important behavioral modifications that are associated with large scale changes in the pattern of gene expression in the brain (e.g. [20, 21, 22]).

Section snippets

Communication between males and females

Before starting a new colony reproductive individuals must find a mating partner. Chemical communication plays a fundamental role in this process and males in particular show numerous adaptations that help them find females [3]. These include large compound eyes, strong wing muscles or antennae with large numbers of odor receptors [23, 24]. Most mating patterns fall into two broad categories, the ‘female calling syndrome’ and the ‘male aggregation syndrome’ [1, 3]. In species with the ‘female

Communication between queen and workers

An important prerequisite for the functioning of social insect colonies is the ability of queens to signal their presence and good health. To this end queens produce a chemical signal that often has several effects, among which are the inhibition of the rearing of new reproductives [6, 37•], attraction of workers to the queen (Figure 1b) [6, 37•], the suppression of worker reproduction [6, 7, 17••, 38, 39, 40] and chemical marking of eggs, which allows workers to recognize whether eggs are

Communication between worker sub-castes

Division of labor among workers is an important reason for the ecological success of social insects [1, 2]. A key challenge for a colony is to allocate an appropriate number of workers to the different tasks. The number of soldiers in a colony, for example, should match the level of threat a colony faces [57, 58]. Research has shown that pheromones that function as negative and positive feedbacks play a crucial role in balancing the number of workers performing different tasks. In honey bees,

Caste specific response to pheromones

Recent research has started to elucidate caste-specific differences in the olfactory system that underlie caste-specific responses to pheromones. For instance, males, queens and workers differ in the number of sensory sensillae on the antennae [69, 70] and in the expression of a range of odorant receptors (ORs), some of which are known to respond to components of queen pheromone [9, 71]. The number of sensory sensillae, in turn, has been shown to correlate with the number of glomeruli, the

Concluding remarks

Communication systems are a prerequisite for the functioning of complex biological systems in general and animal societies in particular. Yet, despite decades of research we still have a superficial understanding of the identity of the chemicals and the corresponding receptors that are involved and their location of action. The development of new molecular tools has started to shed light on these mechanistic questions and future work will allow us to gain a better understanding of how systems

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Conflict of interest statement

Nothing declared.

Acknowledgements

This work was supported by a Swiss NSF grant (Ambizione Fellowship grant no.: PZOOP3_142628/1) to C.G. and several grants from the Swiss NSF and an advanced ERC grant to L.K.

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    Present address: Institute of Zoology, Johannes Gutenberg University Mainz, Johannes von Müller Weg 6, 55099 Mainz, Germany.

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