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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.
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The effect of the brood and the queen on early gene expression in bumble bee workers' brains
Abstract Worker reproduction in social insects is often regulated by the queen, but can be regulated by the brood and nestmates, who may use different mechanisms to induce the same outcomes in subordinates. Analysis of brain gene expression patterns in bumble bee workers (Bombus impatiens) in response to the presence of the queen, the brood, both or neither, identified 18 differentially expressed genes, 17 of them are regulated by the queen and none are regulated by the brood. Overall, brain gene expression differences in workers were driven by the queen’s presence, despite recent studies showing that brood reduces worker egg laying and provides context to the queen pheromones. The queen affected important regulators of reproduction and brood care across insects, such asneuroparsinandvitellogenin, and a comparison with similar datasets in the honey bee and the clonal raider ant revealed thatneuroparsinis differentially expressed in all species. These data emphasize the prominent role of the queen in regulating worker physiology and behavior. Genes that serve as key regulators of workers’ reproduction are likely to play an important role in the evolution of sociality.
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- Award ID(s):
- 1942127
- PAR ID:
- 10363154
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 12
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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