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

Abstract

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.

Biogeographic–tectonic calibration of 14 nodes in a butterfly timetree

“…Most current studies of biogeography use the same method to analyse spatial aspects of evolution (adopting a priori areas and using one or more "ancestral area" algorithms), and the same method to establish the time line of evolution (using fossil calibrations to give maximum clade ages). This is seen in many recent studies on Lepidoptera (for example, Kodandaramaiah et al, 2018;Toussaint et al, 2019Toussaint et al, , 2021aToussaint et al, , 2021bCrews and Esposito, 2020;Chazot et al, 2021;Krupitsky et al, 2021;Matos-Marav ı et al, 2021;Usami et al, 2021;Zhao et al, 2022;St Laurent et al, 2023). Biogeography would benefit from a greater diversity of approaches, as the current methods of area analysis and dating analysis have serious shortcomings (see introductory sections, above).…”

“…Despite these drawbacks, most current studies of biogeographic evolution rely on the ancestral-area algorithms and do not examine the details of distribution or even map the recovered clades (e.g. for butterflies, Kodandaramaiah et al, 2018;Toussaint et al, 2019Toussaint et al, , 2021aToussaint et al, , 2021bChazot et al, 2021;Condamine et al, 2023;Krupitsky et al, 2021;Matos-Marav ı et al, 2021;Usami et al, 2021;Zhao et al, 2022). Instead, the distributions are analysed with respect to a small number of large, a priori regions, the small number being imposed by computational limits.…”

Climate, immigration and speciation shape terrestrial and aquatic biodiversity in the European Alps

“…We only used trees containing at least 50% of the valid species in the correspondent clade (electronic supplementary material, table S12). For the majority of butterflies and amphibians, we relied on two recently published super-trees [60,61], but for specific butterfly lineages underrepresented in the super-tree, we used complementary phylogenies [62][63][64][65]. To include Alpine species that were absent from these trees, we performed additional calibrations using secondary calibration points.…”

Diapause-Linked Gene Expression Pattern and Related Candidate Duplicated Genes of the Mountain Butterfly Parnassius glacialis (Lepidoptera: Papilionidae) Revealed by Comprehensive Transcriptome Profiling

“…The genus Parnassius is a typical mountain-adapted butterfly group, mainly distributed across the Holarctic, with its highest diversity on the Qinghai–Tibet Plateau (QTP) and adjacent mountainous regions (including Xinjiang and Gansu, China), with a broad elevational range of 3000–5000 m ( Figure 1 ). Previous studies have indicated that the diversification of Parnassius initiated during the Middle Miocene, correlated with their host plant’s spatiotemporal distributions, and geological and paleoenvironmental changes in the QTP region [ 12 , 13 ], as well as the fact that both the ancient gene introgression and climate cooling after the Middle Miocene Climate Optimum (MMCO) might have contributed to the spread of Parnassius species to different altitudes, accompanied by the dispersal from West China to Northeast China and other areas of East Asia [ 14 ]. Among them, the Glacial Apollo butterfly, Parnassius glacialis , is the only species that has dispersed into the southeastern areas of the Yangtze River, and mainly inhabits low-altitude mountains (~200 to 1800 m), suggesting their extraordinary flexibility to local seasonal environmental challenges.…”