Temporal reproductive plasticity is a central life-history trait for most iteroparous animals, yet its underlying molecular mechanisms remain poorly understood. We utilize the reversible reproductive arrest experienced by honey bee queens during colony swarming to investigate how these reproductive specialists dynamically adapt their physiology. We demonstrate that pre-swarming nutritional restriction triggers a resource reallocation, whereby ovarian mass declines as flight muscle function is enhanced, providing empirical support for a flight-fecundity trade-off. This transition is accompanied by elevated juvenile hormone and suppressed ecdysteroid and vitellogenin levels, together with the engagement of three spatially distinct oogenesis checkpoints. These checkpoints engage programmed cell death pathways: autophagy predominates in germarial stem cells and follicle cells, while apoptosis is the primary mechanism in vitellarium oocytes and nurse cells, collectively orchestrating oogenesis arrest. Integrated whole-transcriptomic and metabolomic analyses revealed broad molecular remodeling, including changes in FoxO-, Notch-, Wnt-, and Hippo-related signatures that accompanied oogenesis suppression. Our results indicate a "nutrition-hormone-checkpoint-programmed cell death" model that links colony-level swarming to individual ovary suppression. This work provides a systematic framework for understanding the molecular regulation of the reversible reproductive plasticity of honey bee queens.
Liu et al. (Mon,) studied this question.