Phylogenomics reveal extensive phylogenetic discordance due to incomplete lineage sorting following the rapid radiation of alpine butterflies (Papilionidae: Parnassius)

Abstract

Under rapid radiation, the earliest components of evolutionary divergence are often difficult to resolve, which were always driven by the characteristics of taxa and the limitations of alternative analytical methods. The origin and radiation of the alpine butterfly Parnassius, a high‐altitude mountainous insect group, can be attributed to the uplift of the Qinghai‐Tibet Plateau. Despite detailed phylogenetic analyses of the genus, deep phylogenetic relationships among the major subgenera remain recalcitrant. In this study, 102 individuals from 10 representative Parnassius species were sampled to resolve the phylogenetic relationships among subgenera based on nuclear and mitochondrial genome datasets. Gene‐tree/species‐tree conflicts were detected by concatenation and multispecies coalescent (MSC) approaches. We recovered a well‐supported species tree, despite these conflicts, and detected considerable phylogenetic discordance among genomic regions. The main explanation for the topological discordance among subgenera was extensive incomplete lineage sorting (ILS), whereas introgression events were not prominent. The origin and explosive radiation of Parnassius (i.e., rapid succession of speciation events) in the late Miocene associated with environmental events on the plateau led to short internal branches, thereby increasing ILS and topological conflicts, especially among closely related subgenera. Our results also suggested that MSC approaches (SNP and AFLP Package for Phylogenetic analysis [SNAPP] and SVDquartets) are accurate and superior to the concatenation approach; in particular, SVDquartets can explicitly accommodate gene‐tree/species‐tree conflicts caused by high ILS and demonstrate strong robustness. Finally, we explored the phylogenomic data by testing multiple sources of phylogenomic conflict to clarify the strengths and limitations of different approaches, while considering phylogenetic signal variation in mitochondrial loci. We anticipate that the phylogeny described here will be the backbone of future evolutionary studies of the genus and will provide insight into phylogenetic discordance due to rapid radiation.

Host genetics and larval host plant modulate microbiome structure and evolution underlying the intimate insect–microbe–plant interactions in Parnassius species on the Qinghai‐Tibet Plateau

“…Left: the phylogenetic tree of 12 populations covering 9 Parnassius species based on the nuclear (37S_no_missing) dataset according to He et al. ( 2023 ); Right: the cluster dendrogram analyzed based on the gut bacterial communities using the Bray–Curtis metric.…”

“…Environmental variables were converted to distance matrices through various means as performed previously (Youngblut et al., 2019 ). Host phylogenetic distance matrices were generated using the Kimura 2‐parameter model with a gamma distribution (shape parameter = 3) in MEGA X (Kumar et al., 2018 ), based on three nucleotide datasets: (1) 37S_missing_0.25 (5,532,419 autosomal single‐nucleotide variants [SNVs]); (2) 37S_no_missing (728,820 SNVs); and (3) 13 mitochondrial protein‐coding genes (13 PCGs, 10,347 bp), all of which were derived from the newly sequenced data of 37 samples in 12 populations covering 9 Parnassius species from our laboratory (Table S12 ) (He et al., 2023 ). The pairwise geographic distance (the great circle route) matrix was calculated using geosphere v1.5‐18 (Hijmans, 2022 ), based on the information of longitude and latitude for each sample.…”

“…Previous studies have suggested that the genus Parnassius probably originated and experienced rapid radiation following the host plant shifts at about 17–13 million years ago during the middle‐to‐late Miocene, with the spatiotemporally evolutionary pattern correlating with the larval host plant's diversification, paleo‐geological, and paleo‐environmental changes on the QTP, supporting the underlying coevolutionary scenario between Parnassius and host plants (Allio et al., 2021 ; Condamine et al., 2018 ; Su et al., 2020 ; Tao et al., 2020 ; Zhao et al., 2022 ), and making them an ideal model for detecting the mechanism of the potential insect–microbe–plant interactions. Recently, extensive phylogenetic discordance (e.g., different tree topologies derived from different nuclear, or mitochondrial concatenated datasets) due to incomplete lineage sorting following the rapid radiation of this alpine butterfly group has been reported (He et al., 2023 ). However, in the process of spatiotemporal diversification, how and when the microbial community structure of this group is shaped, that is to say, it is shaped by host genetic background (phylosymbiosis) or by other factors is not yet addressed.…”

A Comprehensive Analysis of Triplophysa labiata (Kessler, 1874) Mitogenome and Its Phylogenetic Implications within the Triplophysa Genus

“…The substantial uplift of the QTP over an extended duration is thought to have exerted a pivotal influence on the emergence and expansion of this genus. This geologically dynamic event is considered to be a key factor contributing to the evolutionary success and diversification of the studied genus [2,3]. The Triplophysa genus demonstrates exceptional adaptability to extreme environments, displaying remarkable temperature tolerance and resistance to desiccation.…”

“…They serve critical functions in regulating energy metabolism, apoptosis, aging, and various Genes 2023, 14, 1356 2 of 12 diseases. Consequently, mitochondria are widely recognized as indispensable components within the cells of most living organisms [3]. Double-stranded mitochondrial DNA (mtDNA) is a valuable molecular marker commonly utilized in systematic studies due to its simple structure, rapid evolutionary rate, abundant copies, and ease of isolation and purification.…”