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Background: The genetic basis of wing development has been well characterised for model insect species, but remains poorly understood in phylogenetically divergent, non-model taxa. Wing-polymorphic insect species potentially provide ideal systems for unravelling the genetic basis of secondary wing reduction. Stoneflies (Plecoptera) represent an anciently derived insect assemblage for which the genetic basis of wing polymorphism remains unclear. We undertake quantitative RNA-seq of sympatric full-winged versus vestigial-winged nymphs of a widespread wing-dimorphic New Zealand stonefly, Zelandoperla fenestrata, to identify genes potentially involved in wing development and secondary wing loss. Results: Our analysis reveals substantial differential expression of wing-development genes between full-winged versus vestigial-winged stonefly ecotypes. Specifically, of 23 clusters showing significant similarity to Drosophila wing development-related genes and their pea aphid orthologues, nine were significantly upregulated in full-winged stonefly ecotypes, whereas only one cluster (teashirt) was substantially upregulated in the vestigial-winged ecotype. Conclusions: These findings suggest remarkable conservation of key wing-development pathways throughout 400 Ma of insect evolution. The finding that two Juvenile Hormone pathway clusters were significantly upregulated in vestigial-winged Zelandoperla supports the hypothesis that Juvenile Hormone may play a key role in modulating insect wing polymorphism, as has previously been suggested for other insect lineages. [ABSTRACT FROM AUTHOR]