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Polyphenism allows organisms to respond to varying environmental conditions by adopting alternative collections of morphological traits, often leading to different reproductive strategies. In many insects, polyphenism affecting the development of flight trades dispersal ability for increased fecundity. The soapberry bug Jadera haematoloma (Hemiptera: Rhopalidae) exhibits wing polyphenism in response to juvenile nutritional resources and cohort density. Development of full-length wings and flight-capable thoracic muscles occurs more frequently in cohorts raised under low food density conditions, and these features are correlated to reduced female fecundity. Soapberry bugs represent an example of polyphenic dispersal-fecundity trade-off. Short-wing development is not sex-limited, and morphs can also differ in male fertility. We have previously shown, via a candidate gene approach, that manipulation of insulin signaling can alter the threshold for nutritional response and that changes in the activity of this pathway underlie, at least in part, differences in the polyphenic thresholds in different host-adapted populations of J. haematoloma. We now expand the examination of this system using transcriptome sequencing across a multidimensional matrix of life stage, tissue, sex, food density, and host population. We also examine the use of wing and thorax shape as factors modeling gene expression. In addition to insulin signaling, we find that components of the TOR, Hippo, Toll, and estrogen-related receptor pathways are differentially expressed in the thorax of polyphenic morphs. The transcription factor Sox14 was one of the few genes differentially expressed in the gonads of morphs, being up-regulated in ovaries. We identify two transcription factors as potential mediators of morph-specific male fertility differences. We also find that bugs respond to nutrient limitation with expression of genes linked to cuticle structure and spermatogenesis. These findings provide a broad perspective from which to view this nutrition-dependent polyphenism.