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Adult Gryllus assimilis given an analog of juvenile hormone exhibited reduced flight muscles and enlarged ovaries similar to those found in naturally occurring flightless individuals of species that are polymorphic for dispersal capability. Control and hormone-treated (flightless) G. assimilis did not differ in the amount of food consumed or assimilated on any of three diets that differed in nutrient quantity. Thus, enhanced ovarian growth of flightless individuals resulted from increased allocation of internal nutrients to reproduction (i.e., a trade-off) rather than from increased acquisition of nutrients. Compared with flight-capable controls, flightless G. assimilis also had reduced whole-organism respiration, reduced respiration of flight muscles, and reduced lipid and triglyceride (flight fuel) reserves. These differences are remarkably similar to those between naturally occurring flightless and flight-capable morphs of other Gryllus species. Results collectively suggest that the increased allocation of nutrients to ovarian growth in flightless G. assimilis and other Gryllus species results from reduced energetic costs of flight-muscle maintenance and/or the biosynthesis or acquisition of lipids. Reduction in these energetic costs appears to be an important driving force in the evolution of flightlessness in insects. Respiratory metabolism associated with flight capability utilizes an increasing proportion of the energy budget of crickets as the quantity of nutrients in the diet is decreased. This leads to a magnification of greater ovarian growth of flightless versus flight-capable individuals on nutrient-poor diets.