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The extent to which modifications in intermediary metabolism contribute to life history variation and trade-offs is an important but poorly understood aspect of life history evolution. Artificial selection was used to produce replicate genetic stocks of the wing-polymorphic cricket, Gryllus firmus, that were nearly pure-breeding for either the flight-capable (LW[f]) morph, which delays ovarian growth, or the flightless (SW) morph, which exhibits enhanced early-age fecundity. LW(f) lines accumulated substantially more triglyceride, the main flight fuel in Gryllus, compared with SW-selected lines, and enhanced accumulation of triglyceride was strongly associated with reduced ovarian growth. Increased triglyceride accumulation in LW(f) lines resulted from elevated de novo biosynthesis of fatty acid and two morph-specific trade-offs: (1) greater proportional utilization of fatty acid for glyceride biosynthesis vs. oxidation, and (2) a greater diversion of fatty acids into triglyceride vs. phospholipid biosynthesis. Even though SW lines produced less total lipid and triglyceride, they produced more phospholipid (important in egg development) than did LW(f) lines. Differences between LW(f) and SW morphs in lipid biosynthesis resulted from substantial alterations in the activities of all studied lipogenic enzymes, a result that is consistent with expectations of Metabolic Control Theory. Finally, application of a juvenile hormone analogue to LW(f) females produced a striking SW phenocopy with respect to all aspects of lipid metabolism studied. Global alterations of lipid metabolism, most likely produced by alterations in endocrine regulation, underlie morph specializations for flight vs. early-age fecundity in G. firmus. Modification of the endocrine control of intermediary metabolism is likely to be an important mechanism by which intermediary metabolism evolves and contributes to life history evolution.