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To explore mechanistic constraints on the evolution of optimal phenotypes, we develop an optimality model for thermoregulation in Colias butterflies. The model identifies the thermoregulatory characteristics of butterflies that maximize time available for flight activity subject to an overheating constraint, and was tested in three Colias populations along an elevational gradient. Model simulations and field results showed that environmental variation limits available flight time in higher elevation populations, even for optimally designed butterflies. Optimal predicted thermoregulatory characteristics were within two standard deviations of the observed characteristics in each population. Model simulations and field transplant experiments showed that large departures from optimality would have deleterious consequences for flight and overheating. This represents the first test of a strategy model for optimal thermoregulatory characteristics in animals. Our results illustrate how the constraints imposed by environmental variation and the mechanisms of adaptation affect the evolution of locally optimal phenotypes. We argue that, used in this mechanistic context, optimality modeling remains a powerful tool in studying adaptation.
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