Animal and human highlanders have evolved distinct traits to enhance tissue oxygen delivery and utilization. Unlike vertebrates, insects use their tracheal system for efficient oxygen delivery. However, the genetic basis of insect adaptation to high-altitude hypoxia remains unexplored. Here, we report a potential mechanism of metabolic adaptation of migratory locusts in the Tibetan Plateau, through whole-genome resequencing and functional investigation. A genome-wide scan revealed that the positively selected genes in Tibetan locusts are predominantly involved in carbon and energy metabolism. We observed a notable signal of natural selection in the gene PTPN1, which encodes PTP1B, an inhibitor of insulin signaling pathway. We show that a PTPN1 coding mutation regulates the metabolism of Tibetan locusts by mediating insulin signaling activity in response to hypoxia. Overall, our findings provide evidence for the high-altitude hypoxia adaptation of insects at the genomic level and explore a potential regulatory mechanism underlying the evolved metabolic homeostasis.

Wing dimorphism, that is, wingless and winged forms, can be induced by maternal stress signals and is an adaptive response of aphids to environmental changes. Here, we investigated the ecological and molecular effects of three kinds of stress, namely crowding, predation, and aphid alarm pheromone, on wing dimorphism. These three stressors induced high proportion of up to 60% of winged morphs in offspring. Transcriptome analysis of stress‐treated female aphids revealed different changes in maternal gene expression induced by the three stressors. Crowding elicited widespread changes in the expression of genes involved in nutrient accumulation and energy mobilization. Distinct from crowding, predation caused dramatic expression changes in cuticle protein (CP) genes. Twenty‐three CP genes that belong to CP RR2 subfamily and are highly expressed in legs and embryos were greatly repressed by the presence of ladybird. By contrast, application of alarm pheromone, E‐β‐farnesene, caused slight changes in gene expression. The three factors shared a responsive gene, cuticle protein 43. This study reveals the adaptive response of aphids to environmental stresses and provides a rich resource on genome‐wide expression genes for exploring molecular mechanisms of ecological adaptation in aphids.OPEN RESEARCH BADGES This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.55b2b15.