The mountain butterfly Parnassius glacialis is a representative species of the genus Parnassius, which probably originated in the high-altitude Qinhai–Tibet Plateau in the Miocene and later dispersed eastward into relatively low-altitude regions of central to eastern China. However, little is known about the molecular mechanisms underlying the long-term evolutionary adaptation to heterogeneous environmental conditions of this butterfly species. In this study, we obtained the high-throughput RNA-Seq data from twenty-four adult individuals in eight localities, covering nearly all known distributional areas in China, and firstly identified the diapause-linked gene expression pattern that is likely to correlate with local adaptation in adult P. glacialis populations. Secondly, we found a series of pathways responsible for hormone biosynthesis, energy metabolism and immune defense that also exhibited unique enrichment patterns in each group that are probably related to habitat-specific adaptability. Furthermore, we also identified a suite of duplicated genes (including two transposable elements) that are mostly co-expressed to promote the plastic responses to different environmental conditions. Together, these findings can help us to better understand this species’ successful colonization to distinct geographic areas from the western to eastern areas of China, and also provide us with some insights into the evolution of diapause in mountain Parnassius butterfly species.

Parnassius butterflies have significantly advanced our understanding of biogeography, insect–plant interactions, and other fields of ecology and evolutionary biology. However, to date, little is known about the gene expression patterns related to the high-altitude adaptation of Parnassius species. In this study, we obtained high-throughput RNA-seq data of 48 adult Parnassius individuals covering 10 species from 12 localities in China, and deciphered their interspecific and intraspecific expression patterns based on comparative transcriptomic analyses. Though divergent transcriptional patterns among species and populations at different altitudes were found, a series of pathways related to genetic information processing (i.e., recombination, repair, transcription, RNA processing, and ribosome biogenesis), energy metabolism (i.e., oxidative phosphorylation, thermogenesis, and the citrate cycle), and cellular homeostasis were commonly enriched, reflecting similar strategies to cope with the high-altitude environments by activating energy metabolism, enhancing immune defense, and concurrently inhibiting cell growth and development. These findings deepen our understanding about the molecular mechanisms of adaptative evolution to extreme environments, and provide us with some theoretical criteria for the biodiversity conservation of alpine insects.