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The hallmark of social insects is their caste system: reproduction is primarily monopolized by queens, whereas workers specialize in the other tasks required for colony growth and survival. Pheromones produced by reining queens have long been believed to be the prime factor inhibiting the differentiation of new reproductive individuals. However, there has been very little progress in the chemical identification of such inhibitory pheromones. Here we report the identification of a volatile inhibitory pheromone produced by female neotenics (secondary queens) that acts directly on target individuals to suppress the differentiation of new female neotenics and identify n-butyl-n-butyrate and 2-methyl-1-butanol as the active components of the inhibitory pheromone. An artificial pheromone blend consisting of these two compounds had a strong inhibitory effect similar to live neotenics. Surprisingly, the same two volatiles are also emitted by eggs, playing a role both as an attractant to workers and an inhibitor of reproductive differentiation. This dual production of an inhibitory pheromone by female reproductives and eggs probably reflects the recruitment of an attractant pheromone as an inhibitory pheromone and may provide a mechanism ensuring honest signaling of reproductive status with a tight coupling between fertility and inhibitory power. Identification of a volatile pheromone regulating caste differentiation in a termite provides insights into the functioning of social insect colonies and opens important avenues for elucidating the developmental pathways leading to reproductive and nonreproductive castes.

By using a functional genomics approach, we have identified a honey bee [Apis mellifera (Am)] odorant receptor (Or) for the queen substance 9-oxo-2-decenoic acid (9-ODA). Honey bees live in large eusocial colonies in which a single queen is responsible for reproduction, several thousand sterile female worker bees complete a myriad of tasks to maintain the colony, and several hundred male drones exist only to mate. The \"queen substance\" [also termed the queen retinue pheromone (QRP)] is an eight-component pheromone that maintains the queen's dominance in the colony. The main component, 9-ODA, acts as a releaser pheromone by attracting workers to the queen and as a primer pheromone by physiologically inhibiting worker ovary development; it also acts as a sex pheromone, attracting drones during mating flights. However, the extent to which social and sexual chemical messages are shared remains unresolved. By using a custom chemosensory-specific microarray and qPCR, we identified four candidate sex pheromone Ors (AmOr10, -11, -18, and -170) from the honey bee genome based on their biased expression in drone antennae. We assayed the pheromone responsiveness of these receptors by using Xenopus oocytes and electrophysiology. AmOr11 responded specifically to 9-ODA (EC₅₀ = 280 ± 31 nM) and not to any of the other seven QRP components, other social pheromones, or floral odors. We did not observe any responses of the other three Ors to any of the eight QRP pheromone components, suggesting 9-ODA is the only QRP component that also acts as a long-distance sex pheromone.

Social insects are known for their reproductive division of labor between queens and workers, whereby queens lay the majority of the colony’s eggs, and workers engage mostly in non-reproductive tasks. Queens produce pheromones that signal their presence and fertility to workers, which in turn generally remain sterile. Recently, it has been discovered that specific queen-characteristic cuticular hydrocarbons (CHCs) function as queen pheromones across multiple lineages of social insects. In the common wasp, Vespula vulgaris , several long-chain linear alkanes and 3-methylalkanes were shown to act as queen signals. Here, we describe similar bioassays with a related species of highly eusocial vespine wasp, the Saxon wasp, Dolichovespula saxonica. We show that a blend of queen-characteristic hydrocarbons that are structurally related to those of the common wasp inhibit worker reproduction, suggesting conservation of queen pheromones across social wasps. Overall, our results highlight the central importance of CHCs in chemical communication among social insects in general, and as conserved queen pheromones in these social wasps in particular.

Abstract In social insects, it has been suggested that reproduction and the production of particular fertility-linked cuticular hydrocarbons (CHC) may be under shared juvenile hormone (JH) control, and this could have been key in predisposing such cues to later evolve into full-fledged queen pheromone signals. However, to date, only few studies have experimentally tested this “hormonal pleiotropy” hypothesis. Here, we formally test this hypothesis using data from four species of Polistine wasps, Polistes dominula, Polistes satan, Mischocyttarus metathoracicus, and Mischocyttarus cassununga, and experimental treatments with JH using the JH analogue methoprene and the anti-JH precocene. In line with reproduction being under JH control, our results show that across these four species, precocene significantly decreased ovary development when compared with both the acetone solvent-only control and the methoprene treatment. Consistent with the hormonal pleiotropy hypothesis, these effects on reproduction were further matched by subtle shifts in the CHC profiles, with univariate analyses showing that in P. dominula and P. satan the abundance of particular linear alkanes and mono-methylated alkanes were affected by ovary development and our hormonal treatments. The results indicate that in primitively eusocial wasps, and particularly in Polistes, reproduction and the production of some CHC cues are under joint JH control. We suggest that pleiotropic links between reproduction and the production of such hydrocarbon cues have been key enablers for the origin of true fertility and queen signals in more derived, advanced eusocial insects.

In eusocial insects the production of daughters is generally restricted to mated queens, and unmated workers are functionally sterile. The evolution of this worker sterility has been plausibly explained by kin selection theory [Hamilton W (1964) J Theor Biol 7:1–52], and many traits have evolved to prevent conflict over reproduction among the females in an insect colony. In honeybees (Apis mellifera), worker reproduction is regulated by the queen, brood pheromones, and worker policing. However, workers of the Cape honeybee, Apis mellifera capensis, can evade this control and establish themselves as social parasites by activating their ovaries, parthenogenetically producing diploid female offspring (thelytoky) and producing queen-like amounts of queen pheromones. All these traits have been shown to be strongly influenced by a single locus on chromosome 13 [Lattorff HMG, et al. (2007) Biol Lett 3:292–295]. We screened this region for candidate genes and found that alternative splicing of a gene homologous to the gemini transcription factor of Drosophila controls worker sterility. Knocking out the critical exon in a series of RNAi experiments resulted in rapid worker ovary activation—one of the traits characteristic of the social parasites. This genetic switch may be controlled by a short intronic splice enhancer motif of nine nucleotides attached to the alternative splice site. The lack of this motif in parasitic Cape honeybee clones suggests that the removal of nine nucleotides from the altruistic worker genome may be sufficient to turn a honeybee from an altruistic worker into a parasite.

Animal nutritional state can profoundly affect behaviour, including an individual's tendency to cooperate with others. We investigated how nutritional restriction at different life stages affects cooperative behaviour in a highly social species, Apis mellifera honeybees. We found that nutritional restriction affects a worker's queen pheromone response, a behavioural indicator of investment in group vs. individual reproduction. Nutritional restriction at the larval stage led to reduced ovary size and increased queen pheromone response, whereas nutritional restriction at the adult stage led to reduced lipid stores and reduced queen pheromone response. We argue that these differences depend upon the extent of reproductive plasticity at these life stages and that individual worker honeybees may adjust their behavioural and physiological traits in response to nutritional stress to invest nutritional resources in either their own or their colony's reproduction. These results support the role of nutritional stress in the maintenance of cooperative behaviour, and we suggest that historical nutritional scarcity may be an important contributor to the evolution of extreme forms of cooperation. A plain language summary is available for this article. Plain Language Summary

The queen mandibular pheromone (QMP) identified from the honeybee is responsible for maintaining reproductive division of labour in the colony, and affects multiple behaviours. Interestingly, QMP inhibits reproduction not only in honeybee workers, but also in distantly related insect species such as fruit flies and bumblebees. This study examines whether QMP also affects worker reproduction in the common wasp Vespula vulgaris. Wasp workers were exposed to one of the following treatments: QMP, wasp queen pheromone (the hydrocarbon heptacosane n-C27), or acetone (solvent-only control). After dissecting the workers, no evidence that QMP inhibits development in V. vulgaris could be found. However, this study could confirm the inhibitory effect of the hydrocarbon heptacosane on ovary activation. The reason why non-social species such as the fruit fly and social species such as bumblebees and ants respond to the QMP, while the social wasp V. vulgaris does not, is unclear. The investigation of whether olfaction is key to sensing QMP in other insect species, and the detailed study of odorant receptors in other social insects, may provide insights into the mechanisms of response to this pheromone.

Pheromones are likely involved in all social activities of social insects including foraging, sexual behavior, defense, nestmate recognition, and caste regulation. Regulation of the number of fertile queens requires communication between reproductive and non-reproductive individuals. Queen-produced pheromones have long been believed to be the main factor inhibiting the differentiation of new reproductive individuals. However, since the discovery more than 50 years ago of the queen honeybee substance that inhibits the queen-rearing behavior of workers, little progress has been made in the chemical identification of inhibitory queen pheromones in other social insects. The recent identification of a termite queen pheromone and subsequent studies have elucidated the multifaceted roles of volatile pheromones, including functions such as a fertility signal, worker attractant, queen–queen communication signal, and antimicrobial agent. The proximate origin and evolutionary parsimony of the termite queen pheromone also are discussed.

Background: Variation in individual behavior within social groups can affect the fitness of the group as well as the individual, and can be caused by a combination of genetic and environmental factors. However, the molecular factors associated with individual variation in social behavior remain relatively unexplored. We used honey bees (Apis mellifera) as a model to examine differences in socially-regulated behavior among individual workers, and used transcriptional profiling to determine if specific gene expression patterns are associated with these individual differences. In honey bees, the reproductive queen produces a pheromonal signal that regulates many aspects of worker behavior and physiology and maintains colony organization. Methodology/Principal Findings: Here, we demonstrate that there is substantial natural variation in individual worker attraction to queen pheromone (QMP). Furthermore, worker attraction is negatively correlated with ovariole number—a trait associated with reproductive potential in workers. We identified transcriptional differences in the adult brain associated with individual worker attraction to QMP, and identified hundreds of transcripts that are organized into statistically-correlated gene networks and associated with this response. Conclusions/Significance: Our studies demonstrate that there is substantial variation in worker attraction to QMP among individuals, and that this variation is linked with specific differences in physiology and brain gene expression patterns. This variation in individual response thresholds may reveal underlying variation in queen-worker reproductive conflict, and may mediate colony function and productivity by creating variation in individual task performance.

Volatile compounds provide important olfactory cues for honey bees ( Apis mellifera L.), which are essential for their ecology, behavior, and social communication. In the external environment bees locate food sources by the use of floral scents, while inside the hive, pheromones such as the queen mandibular pheromone (QMP) and alarm pheromones serve important functions in regulating colony life and inducing aggressive responses against intruders and parasites. Widely reported alterations of various behaviors in- and outside the hive following exposure to pesticides could therefore be associated with a disturbance of odor sensitivity. In the present study, we tested the effects of neonicotinoid pesticides at field concentrations on the ability of honey bees to perceive volatiles at the very periphery of the olfactory system. Bee colonies were subjected to treatments during the summer with either Imidacloprid or Thiacloprid at sublethal concentrations. Antennal responses to apple ( Malus domestica L.) flower volatiles were studied by GC-coupled electro-antennographic detection (GC-EAD), and a range of volatiles, a substitute of the QMP, and the alarm pheromone 2-heptanone were tested by electroantennography (EAG). Short-term and long-term effects of the neonicotinoid treatments were investigated on bees collected in the autumn and again in the following spring. Treatment with Thiacloprid induced changes in antennal responses to specific flower VOCs, with differing short- and long-term effects. In the short term, increased antennal responses were observed for benzyl-alcohol and 1-hexanol, which are common flower volatiles but also constituents of the honey bee sting gland secretions. The treatment with Thiacloprid also affected antennal responses to the QMP and the mandibular alarm pheromone 2-heptanone. In the short term, a faster signal degeneration of the response signal to the positive control citral was recorded in the antennae of bees exposed to Thiacloprid or Imidacloprid. Finally, we observed season-related differences in the antennal responses to multiple VOCs. Altogether, our results suggest that volatile-specific alterations of antennal responses may contribute to explaining several behavioral changes previously observed in neonicotinoid-exposed bees. Treatment effects were generally more prominent in the short term, suggesting that adverse effects of neonicotinoid exposure may not persist across generations.