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Flight muscles of the cricket Gryllus firmus are polymorphic, existing as pink or white phenotypes. White muscles are smaller in size, have reduced number and size of muscle fibers, and have reduced in vitro enzyme activities and respiration rates relative to pink muscles of newly molted, fully winged adults. G. firmus is also polymorphic for wing length. All newly molted long-winged adults exhibited the pink-muscle phenotype, while most newly molted short-winged adults exhibited the white-muscle phenotype, which resulted from arrested muscle growth. As long-winged adults aged, fully grown pink muscle was transformed into white muscle via histolysis. The substantially higher respiration rate of pink muscle likely contributes to the elevated whole-organism respiration rate of long-winged females, which has been documented previously and which is thought to divert nutrients from egg production. Histolyzed white flight muscle from long-winged crickets also exhibited significantly elevated respiration rate and enzyme activities compared with underdeveloped white muscle from short-winged adults, although these differences were not as great as those between pink and white muscles. Fecundity was much more elevated in females with white versus pink flight muscles than it was in females with short versus long wings. The fitness gain resulting from flightlessness has typically been estimated in previous studies by comparing enhanced egg production of short-winged and long-winged females, without considering the influence of flight-muscle variation. Our results suggest that the magnitude of this fitness gain has been substantially underestimated.