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Adaption to dietary changes is critical to understanding evolution of host plant ranges in polyphagous insects. We compared three taxa of lepidopteran herbivores from the predominantly generalist genus Spodoptera showing different degrees of polyphagy: S. littoralis, with a broad host range including both mono- and dicotyledonous plants, and two strains [Corn (i.e. maize) (C) and Rice (R)] of S. frugiperda adapted primarily to different grass species. Larval performance of the three taxa was compared in a feeding bioassay on artificial pinto diet and maize leaves. On pinto diet all taxa showed good performance, while on maize the two taxa non-specialised on maize showed lower survival, growth rate, and pupal weight compared to the maize-specialist S. frugiperda C-strain. The differential metabolic responses after feeding on the two diets were characterized with RNA-Seq analysis of midgut transcriptomes from the 3rd instar larvae. The generalist S. littoralis showed broader transcriptional readjustments compared with the maize-specialist S. frugiperda C-strain after feeding on maize. Substantial alteration in the expression levels of digestive and detoxifying enzymes, transporters, immunity, and peritrophic membrane associated transcripts was also documented in all the taxa to overcome maize defences. However, the expression level of detoxifying enzymes like UDP glucosyl transferases, which detoxify the most abundant maize leaf toxin 2, 4-dihydroxy-7-methoxy-1, 4-benzoxazin-3-one (DIMBOA), did not alter significantly after feeding on maize. High background expression level of UDP –glucosyl transferases was documented in the maize specialist S. frugiperda C-strain contributing to its fitness on maize. Altogether, these findings provide compelling evidence for divergent diet specific remodelling of digestive physiology among these three Spodoptera taxa. Moreover, the comparisons between the C and R- strain of S. frugiperda fed on the same diet revealed significant genetic divergence among these two closely related strains. |