Phylogeography and ecological niche modeling implicate multiple microrefugia of Swertia tetraptera during quaternary glaciations

Abstract

Background: Climate fluctuations during the Pleistocene and mountain uplift are vital driving forces affecting geographic distribution. Here, we ask how an annual plant responded to the Pleistocene glacial cycles.

Methods: In this study, we analyzed the population demographic history of the annual herb Swertia tetraptera Maxim (Gentianaceae) endemic to Qinghai-Tibetan Plateau (QTP). A total of 301 individuals from 35 populations of S. tetraptera were analyzed based on two maternally inherited chloroplast fragments (trnL-trnF and trnS-trnG). Phylogeographic analysis was combined with species distribution modeling to detect the genetic variations in S. tetraptera.

Results: The genetic diversity of S. tetraptera was high, likely due to its wide natural range, high proportion of endemic haplotypes and evolutionary history. Fifty-four haplotypes were identified in S. tetraptera. Only a few haplotypes were widespread (Hap_4, Hap_1, Hap_3), which were dispersed throughout the present geographical range of S. tetraptera, while many haplotypes were confined to single populations. The cpDNA dataset showed that phylogeographic structuring was lacking across the distribution range of S. tetraptera. Analyses of molecular variance showed that most genetic variation was found within populations (70.51%). In addition, the relationships of the haplotypes were almost completely unresolved by phylogenetic reconstruction. Both mismatch distribution analysis and neutrality tests showed a recent expansion across the distribution range of S. tetraptera. The MaxEnt analysis showed that S. tetraptera had a narrow distribution range during the Last Glacial Maximum (LGM) and a wide distribution range during the current time, with predictions into the future showing the distribution range of S. tetraptera expanding.

Conclusion: Our study implies that the current geographic and genetic distribution of S. tetraptera is likely to have been shaped by Quaternary periods. Multiple microrefugia of S. tetraptera existed during Quaternary glaciations. Rapid intraspecific diversification and hybridization and/or introgression may have played a vital role in shaping the current distribution patterns of S. tetraptera. The distribution range of S. tetraptera appeared to have experienced contraction during the LGM; in the future, when the global climate becomes warmer with rising carbon dioxide levels, the distribution of S. tetraptera will expand.

Keywords: Haplotypes; Phylogeographic structure; Qinghai-Tibetan Plateau; Quaternary glaciations; Refugia; Swertia tetraptera; cpDNA trnS-trnG.

Fig. 1

A, map of China, indicating the Qinghai-Tibetan Plateau (Green) and the distribution range of Swertia tetraptera. B, map of the 35 sampled populations of Swertia tetraptera and the distribution of cpDNA haplotypes in the species. Pie charts show the proportions of haplotypes within each population. The codes of populations are the same as in Table 1. (Note: The background map is taken from an open-access dataset, Integration dataset of Tibet Plateau boundary. National Tibetan Plateau Data Center. Zhang, Y. (2019). Integration dataset of Tibet Plateau boundary. National Tibetan Plateau Data Center. 10.11888/Geogra.tpdc.270099. https://cstr.cn/18406.11.Geogra.tpdc.270099.)

Fig. 2

Phylogenetic tree for 54 cpDNA haplotypes using Bayesian inference (BI) method. Posterior probabilities are shown above the branches. A and B represent two different branches

Fig. 3

MP median-joining network of the 54 cpDNA haplotypes. Circle size is proportional to haplotype frequencies and the red dot represent missing haplotypes. Each color denotes one population of S. tetraptera. The numbers on the branches indicate the number of steps separating adjacent haplotypes

Fig. 4

Mismatch distribution of Swertia tetraptera in the overall populations based on cpDNA dataset

Fig. 5

Predicted distribution of S. tetraptera based on Present (A), LGM (B) and Future (C) bioclimatic data. The highest probability of occurrence was shown in red color, while the lowest probability of occurrence was shown in green color. (Note: The background map is taken from an open-access dataset, Integration dataset of Tibet Plateau boundary. National Tibetan Plateau Data Center. Zhang, Y. (2019). Integration dataset of Tibet Plateau boundary. National Tibetan Plateau Data Center. 10.11888/Geogra.tpdc.270099. https://cstr.cn/18406.11.Geogra.tpdc.270099.)

Fig. 6

Changes in the distribution of suitable habitats of S. tetraptera. The green area indicates that the distribution area of S. tetraptera expands in the later period compared with the previous period; the blue area indicates that the distribution area shrinks compared with the previous period; the gray area indicates that there is no distribution in both periods; and the yellow area indicates that there is potential distribution of S. tetraptera in both periods. (Note: The background map is taken from an open-access dataset, Integration dataset of Tibet Plateau boundary. National Tibetan Plateau Data Center. Zhang, Y. (2019). Integration dataset of Tibet Plateau boundary. National Tibetan Plateau Data Center. 10.11888/Geogra.tpdc.270099. https://cstr.cn/18406.11.Geogra.tpdc.270099.)