In species in which males are free to dynamically alter their allocation to sexual signaling over the breeding season, the optimal investment in signaling should depend on both a male’s state and the level of competition he faces at any given time. We developed a dynamic optimization model within a game‐theoretical framework to explore the resulting signaling dynamics at both individual and population levels and tested two key model predictions with empirical data on three‐spined stickleback (Gasterosteus aculeatus) males subjected to dietary manipulation (carotenoid availability): (1) fish in better nutritional condition should be able to maintain their signal for longer over the breeding season, resulting in an increasingly positive correlation between nutritional status and signal (i.e., increasing signal honesty), and (2) female preference for more ornamented males should thus increase over the breeding season. Both predictions were supported by the experimental data. Our model shows how such patterns can emerge from the optimization of resource allocation to signaling in a competitive situation. The key determinants of the honesty and dynamics of sexual signaling are the condition dependency of male survival, the initial frequency distribution of nutritional condition in the male population, and the cost of signaling
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