Mating triggers a physiological switch to reproduction in field crickets to mitigate the flight-oogenesis tradeoff.

Organisms must reallocate limited resources to meet changing physiological demands, yet the cues that trigger these shifts and the physiological programs that mediate them remain poorly understood. For example, in some winged animals, females cannot simultaneously invest in energetically expensive flight musculature and egg production, requiring physiological transitions between dispersal and reproductive phases of their life cycle (the flight-oogenesis trade-off). However, the mechanisms that allow individuals to transition between dispersal and reproductive states remain unclear. Here, we test whether mating acts as a key external cue that reprograms internal resource allocation from somatic maintenance to reproduction. Using the wing-dimorphic California variable field cricket, Gryllus lineaticeps, we show that mating initiates flight muscle histolysis in long-winged females, eliminating any delay in early-life fecundity. Mating activates transcriptional programs associated with autophagy, iron mobilization, and endocrine signaling, consistent with a coordinated physiological shift that redirects nutrients from flight tissues to oogenesis. These mating-induced changes include altered insulin-like peptide and juvenile hormone signaling, suggesting that conserved hormonal pathways may be repurposed to govern life-history transitions. Together, our findings reveal that mating can serve as a potent trigger for reorganizing nutrient use and physiological priorities, enabling organisms to minimize the reproductive costs of non-reproductive states. By identifying a socially derived cue that initiates state transitions, this work provides a mechanistic framework for understanding how reproductive behaviors drive life-history strategies, and challenges long-standing assumptions about the inherent costs of dispersal.