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The biochemical basis of specializations for dispersal vs. reproduction is an understudied aspect of dispersal polymorphism in insects. Using a radiolabelled amino acid, we quantified differences in in vivo amino acid metabolism between morphs of the wing-polymorphic cricket, Gryllus firmus, that trade-off early age reproduction and dispersal capability. Studies were conducted in crickets fed a variety of diets expected to influence amino acid and lipid metabolism. On the day of molt to adulthood, prior to the morph-specific trade-off between ovarian growth and biochemical preparation for flight (e.g. biosynthesis of triglyceride flight fuel), morphs did not differ in any aspect of amino acid metabolism. However, on day 5 of adulthood, when the morph-specific trade-off between ovarian growth and flight fuel production was manifest, the morphs differed substantially in each of the three aspects of amino acid metabolism studied: conversion to protein, oxidation, and conversion to lipid. Morphs also differed in degree of allocation of products of amino acid metabolism to ovaries vs. the soma. Most importantly, morphs differed in the relative metabolism of radiolabelled glycine through these pathways (i.e. biochemical trade-offs), and in the relative allocation of end products of amino acid metabolism to the soma vs. ovaries (allocation trade-offs). A functionally important interaction between amino acid and lipid metabolism was noted: greater oxidation of amino acids in the flight-capable morph spared fatty acids for enhanced conversion into triglyceride flight fuel. By contrast, greater oxidation of fatty acids by the flightless morph spared amino acids for enhanced conversion into ovarian protein. Diet significantly affected amino acid metabolism. However, MORPH×DIET interactions were rare and morphs differed in amino acid metabolism to a similar degree under the range of diets tested.