Phylogeny and Biogeographic History of Parnassius Butterflies (Papilionidae: Parnassiinae) Reveal Their Origin and Deep Diversification in West China.

Abstract

Simple SummaryButterflies of the genus Parnassius are distributed in the mountains across the Northern Hemisphere. Studies have shown that this genus originated in the regions of West China–Central Asia. To further explore the spatiotemporal pattern and driving mechanism of Parnassius diversification, we reconstructed the phylogeny and biogeographic history of Parnassius based on 45 species. Ancestral area reconstruction obtained by using the statistical dispersal–extinction cladogenesis model indicated that Parnassius originated in West China (Qinghai–Tibet Plateau and Xinjiang) during the Middle Miocene. Paleoenvironment changes and host plants were probably influenced by the dispersal of Parnassius butterflies from West China to East Asia, Europe, and North America. Furthermore, ancient gene introgression might have contributed to the spread of Parnassius butterflies from the high mountains of the Qinghai–Tibet Plateau to the low-altitude areas of Central East China. This study will provide an understanding of the phylogeny and biogeographic history of the genus Parnassius.We studied 239 imagoes of 12 Parnassius species collected from the mountains of the Qinghai–Tibet Plateau (QTP) and its neighbouring areas in China. We selected three mitochondrial gene (COI, ND1, and ND5) sequences, along with the homologous gene sequences of other Parnassius species from GenBank, to reconstruct the phylogenetic tree and biogeographic history of this genus. Our results show that Parnassius comprises eight monophyletic subgenera, with subgenus Parnassius at the basal position; the genus crown group originated during the Middle Miocene (ca. 16.99 Ma), and species diversification continued during sustained cooling phases after the Middle Miocene Climate Optimum (MMCO) when the QTP and its neighbouring regions experienced rapid uplift and extensive orogeny. A phylogenetic network analysis based on transcriptomes from GenBank suggests that ancient gene introgression might have contributed to the spread of the Parnassius genus to different altitudes. Ancestral area reconstruction indicates that Parnassius most likely originated in West China (QTP and Xinjiang) and then spread to America in two dispersal events as subgenera Driopa and Parnassius, along with their host plants Papaveraceae and Crassulaceae, respectively. Our study suggests that extensive mountain-building processes led to habitat fragmentation in the QTP, leading to the early diversification of Parnassius, and climate cooling after MMCO was the driving mechanism for the dispersal of Parnassius butterflies from West China to East Asia, Europe, and North America.