An overlooked dispersal route of Cardueae (Asteraceae) from the Mediterranean to East Asia revealed by phylogenomic and biogeographical analyses of Atractylodes

Abstract

Background and aims: The East Asian-Tethyan disjunction pattern and its mechanisms of formation have long been of interest to researchers. Here, we studied the biogeographical history of Asteraceae tribe Cardueae, with a particular focus on the temperate East Asian genus Atractylodes DC., to understand the role of tectonic and climatic events in driving the diversification and disjunctions of the genus.

Methods: A total of 76 samples of Atractylodes from 36 locations were collected for RAD-sequencing. Three single nucleotide polymorphism (SNP) datasets based on different filtering strategies were used for phylogenetic analyses. Molecular dating and ancestral distribution reconstruction were performed using both chloroplast DNA sequences (127 Cardueae samples) and SNP (36 Atractylodes samples) datasets.

Key results: Six species of Atractylodes were well resolved as individually monophyletic, although some introgression was identified among accessions of A. chinensis, A. lancea and A. koreana. Dispersal of the subtribe Carlininae from the Mediterranean to East Asia occurred after divergence between Atractylodes and Carlina L. + Atractylis L. + Thevenotia DC. at ~31.57 Ma, resulting in an East Asian-Tethyan disjunction. Diversification of Atractylodes in East Asia mainly occurred from the Late Miocene to the Early Pleistocene.

Conclusions: Aridification of Asia and the closure of the Turgai Strait in the Late Oligocene promoted the dispersal of Cardueae from the Mediterranean to East China. Subsequent uplift of the Qinghai-Tibet Plateau as well as changes in Asian monsoon systems resulted in an East Asian-Tethyan disjunction between Atractylodes and Carlina + Atractylis + Thevenotia. In addition, Late Miocene to Quaternary climates and sea level fluctuations played major roles in the diversification of Atractylodes. Through this study of different taxonomic levels using genomic data, we have revealed an overlooked dispersal route between the Mediterranean and far East Asia (Japan/Korea) via Central Asia and East China.

Keywords: Atractylodes; Cardueae; East Asian–Tethyan disjunction; biogeography; phylogenomics.

Fig. 1.

Geographical information of the 36 populations of Atractylodes used for RAD-sequencing (see Supplementary Data Table S1 for precise location information).

Fig. 2.

Maximum-likelihood (ML) phylograms of Atractylodes generated from three RAD-seq matrices differing in the maximum dataset that includes all loci shared across at least 10 (D1), 30 (D2) and 45 (D3) samples. ML bootstrap support >80 % is reported at nodes. Two samples of A. ovata are underlined. Asterisks on the nodes mean bootstrap support = 100%.

Fig. 3.

Chronogram showing the Bayesian consensus tree of 36 Atractylodes samples based on SNP-derived dataset D4 and Bayesian binary MCMC (BBM)-derived reconstruction of biogeographical history. The three distribution areas of Atractylodes used in the Bayes-based biogeographical reconstruction are: A, East China; B, Northeast Asia; and C, Japan. The box with number 1 indicates the secondary calibration point for the crown age of Atractylodes estimated from BEAST analysis of a cpDNA dataset. Nodes N1–N12 show crown ages (95 % highest posterior density) for the divergence time of each major clade. Pie diagrams at internal nodes indicate the relative probabilities for each alternative area.