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The flight-capable morph of the wing-polymorphic cricket, Gryllus firmus, accumulated a substantially greater quantity of total lipid and triglyceride, compared with the obligately flightless morph, during the first five days of adulthood. Increased lipid accumulation in the flight-capable morph was genetically based, and was produced when ovarian growth is substantially reduced in that morph. Temporal changes in lipid levels suggest that the higher triglyceride reserves in the flight-capable morph fed a high-nutrient diet were produced by elevated lipid biosynthesis. By contrast, on a low-nutrient or high carbohydrate diet, increased lipid levels in the flight-capable morph appeared to result primarily from decreased lipid utilization. Increased biosynthesis or retention of triglyceride (the major flight fuel in Gryllus) by the flight-capable morph may significantly divert nutrients from egg production and hence may be an important physiological cause of its reduced ovarian growth. The obligately flightless morph allocated a greater proportion of total lipid to phospholipid than did the flight-capable morph. No functionally-significant differences in total lipid or triglyceride were produced between morphs during the last nymphal stadium. A second flightless morph, derived from the flight-capable morph by histolysis of flight muscles during adulthood, also had reduced amounts of total lipid and triglyceride but increased ovarian growth compared with the flight capable morph on the standard (high-nutrient) diet. Important qualitative and quantitative aspects of lipid metabolism differ genetically between the flight-capable and flightless morphs of G. firmus and likely contribute importantly to their respective adaptations for flight capability vs. reproduction. This is the first study to document genetically-based differences in energy reserves between morphs of a complex (phase, caste, flight) polymorphism in which morphs also differ genetically in key life history traits.