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Abstract Queen pheromones have long been studied as a major factor regulating reproductive division of labor in social insects. Hitherto, only a handful of queen pheromones were identified and their effects on workers have mostly been studied in isolation from the social context in which they operate. Our study examined the importance of behavioral and social context for the perception of queen semiochemicals by bumble bee workers. Our results indicate that a mature queen’s cuticular semiochemicals are capable of inhibiting worker reproduction only when accompanied by the queen’s visual presence and the offspring she produces, thus, when presented in realistic context. Queen’s chemistry, queen’s visual presence and presence of offspring all act to regulate worker reproduction, but none of these elements produces an inhibitory effect on its own. Our findings highlight the necessity to reconsider what constitutes a queen pheromone and suggest a new approach to the study of chemical ecology in social insects. 

Abstract Reproductive division of labor in insect societies is regulated through multiple concurrent mechanisms, primarily chemical and behavioral. Here, we examined if the Dufour’s gland secretion in the primitively eusocial bumble beeBombus impatienssignals information about caste, social condition, and reproductive status. We chemically analyzed Dufour’s gland contents across castes, age groups, social and reproductive conditions, and examined worker behavioral and antennal responses to gland extracts. We found that workers and queens each possess caste-specific compounds in their Dufour’s glands. Queens and gynes differed from workers based on the presence of diterpene compounds which were absent in workers, whereas four esters were exclusive to workers. These esters, as well as the total amounts of hydrocarbons in the gland, provided a separation between castes and also between fertile and sterile workers. Olfactometer bioassays demonstrated attraction of workers to Dufour’s gland extracts that did not represent a reproductive conflict, while electroantennogram recordings showed higher overall antennal sensitivity in queenless workers. Our results demonstrate that compounds in the Dufour’s gland act as caste- and physiology-specific signals and are used by workers to discriminate between workers of different social and reproductive status. 

Abstract Access to reproduction is determined by an individual’s dominance rank in many species and is achieved through aggression and/or dominance signaling. In eusocial insects, one or several dominant females (queens) monopolize reproduction but to what extent queens rely on aggression and signaling remains obscure. Aggression is costly and its efficiency depends on the group size, whereas signaling may reduce the risks and costs of aggression. Both strategies are used to regulate reproduction in social taxa, with aggression being more common in small social groups, compared to signaling in larger societies. Here, we examine the use of aggression and chemical signaling in a social species (Bombus impatiens) where the dominant queen interacts with increasing numbers of workers as she ages. We found that the queen’s strategy to monopolize reproduction changes with life stage, shifting from overt aggression to chemical signaling as the queen gets older. Particularly, old queens exhibited a higher ratio of short to long cuticular hydrocarbons compared to young queens, an endogenous shift that was attributed to age, as all egg-laying queens were fecund and kept with the same number of workers. Our findings contribute to the understanding of reproductive dominance in the context of an individual’s life history. 

The mechanisms that maintain reproductive division of labor in social insects are still incompletely understood. Most studies focus on the relationship between adults, overlooking another important stakeholder– the juveniles. Recent studies show that not only the queen, but also the brood regulate worker reproduction. However, how the two coordinate to maintain reproductive monopoly remained unexplored. Here, we disentangled the roles of the brood and the queen in primitively eusocial bees (Bombus impatiens) by examining their separated and combined effects on worker behavioral, physiological and brain gene expression. We found that young larvae produce a releaser effect on workers, decreasing oviposition and aggression, while the queen produces both releaser and primer effects, modifying worker behaviors and reproductive physiology. The expression of reproduction- and aggression-related genes was altered in the presence of both queen and brood but was stronger or the same in the presence of the queen. We identified two types of interactions between the queen and the brood in regulating worker reproduction: (1) synergistic interactions regulating worker physiology, where the combined effect of the queen and the brood on worker physiology was greater than their separate effects; (2) additive interactions where the combined effect of the queen and the brood on worker behavior was similar to the sum of their separate effects. Our results suggest that the queen and the brood interact synergistically and additively to regulate worker behavior and reproduction, and this interaction exists at multiple regulatory levels.