Table of Contents
  • Volume 50 Issue 4

    Special issue: Phylogeographic studies of plants in China

    Cover illustration: Potential major refugia recovered for Chinese plants. See Editorial by LIU et al., pp. 267–275 in this issue.
    • Jian-Quan LIU, Yong-Shuai SUN, Xue-Jun GE, Lian-Ming GAO, Ying-Xiong QIU
      2012, 50 (4): 267–275
      Abstract   |   References   |   Full Text HTML   |   Full Text PDF   |   Save
      Phylogeography has been one major focus of evolutionary biology in recent years, with many important advances in Chinese species. In this issue, we collected 11 phylogeographic studies of plants by Chinese laboratories. We further synthesized the main findings and patterns emerging from these and previous phylogeographic studies in China and asked where phylogeographic research should be directed in the coming years. Numerous examples have shown that phylogeographic patterns in China did not show an expected expansion–contraction pattern at large scale, mirroring the geological records showing that no unified ice sheet had developed in China during the Quaternary Period. Instead, regional expansions and intraspecific divergences are very common in most studied species during the Quaternary oscillations. Different intraspecific lineages or alleles (haplotypes) were detected in multiple localized refugia, from where regional or local expansions are likely to have started. Hybridizations and introgressions are frequent between intraspecific lineages or between different species. We also reviewed computational methods for phylogeographic analyses. Despite the great progress made in recent years, there remains much to discover about the spatial–temporal dimensions and underlying speciation mechanisms of Chinese plants. Phylogeographic studies represent a key knot that connects the genus phylogeny (macroevolution) and speciation and adaptation (microevolution). Therefore, we advocate that: (i) phylogeographic studies of plants in China should be directed to the closely related species or a monophyletic group (for example, a genus or a section) in the coming years; and (ii) population genetic data based on direct sequencing multiple loci, especially those from nuclear genome and statistical tests should be widely adopted and enforced. The recovered intraspecific divergences and phylogeographic patterns of multiple-species may allow us to better understand the high plant diversity in China and set up concrete hypotheses for studying plant speciation and diversification mechanisms in this region.
    • Research Articles
    • Fa-Qi ZHANG,Qing-Bo GAO,De-Jun ZHANG,Yi-Zhong DUAN,Yin-Hu LI,Peng-Cheng FU,Rui XING,Khan GULZAR,Shi-Long CHEN
      2012, 50 (4): 276–283
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      The aim of the present study was to investigate the phylogeographic patterns of Spiraea alpina (Rosaceae) and clarify its response to past climatic changes in the climate-sensitive Qinghai-Tibetan Plateau (QTP). We sequenced a chloroplast DNA fragment (trnLtrnF) from 528 individuals representing 43 populations. We identified 10 haplotypes, which were tentatively divided into three groups. These haplotypes or groups were distributed in the different regions of the QTP. Only half the populations were fixed by a single haplotype, whereas the others contained two or more. In the central and eastern regions, adjacent populations at the local scale shared the same haplotype. Our phylogeographic analyses suggest that this alpine shrub survived in multiple refugia during the Last Glacial Maximum and that earlier glaciations may have trigged deep intraspecific divergences. Post-glacial expansions occurred only within populations or across multiple populations within a local range. The findings of the present study together with previous phylogeographic reports suggest that evolutionary histories of plants in the QTP are complex and variable depending on the species investigated.
    • Xiu-Feng XIE, Hai-Fei YAN, Feng-Ying WANG, Xue-Jun GE, Chi-Ming HU, Gang HAO
      2012, 50 (4): 284–294
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      To investigate the mechanisms responsible for the high diversity in central and adjacent southwestern China, we inferred the phylogeographic history of Primula ovalifolia from chloroplast DNA data. One hundred and thirty five individuals from 13 natural populations (including one Primula tardiflora population) were analyzed. A total of 23 haplotypes were identified. Most of them were exclusive to a single population. Strong phylogeography structure was detected, with NST (0.936) significantly higher than GST (0.784). Phylogenetic analysis showed that all haplotypes were clustered into three lineages (clades I, II, and III). High genetic diversity was revealed, possibly due to the interglacial contraction and glacial expansion. The three identified lineages may have undergone different historical processes after the mid-Pleistocene, due to their early divergent time. Multiple refugia were inferred for the three lineages. Pleistocene climatic oscillations, combined with the complex local topography, were responsible for the strong phylogeographic pattern of P. ovalifolia. Our analysis supports the hypothesis that the central and adjacent southwestern region of China was an important refugium for the survival, persistence, and further speciation of most East Asia flora, which has led to high species diversity in this region.
    • Hong-Xiang ZHANG, Ming-Li ZHANG
      2012, 50 (4): 295–304
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      Clematis sibirica, a woody vine occurring primarily under conifer forests, is widespread in northern Eurasia. In this study, we intend to illustrate how the taxon has responded in the area of the Tianshan and Altai Mountains of Central Asia to the Pleistocene climatic fluctuations. The chloroplast intergenic spacer psbA-trnH was sequenced for 125 individuals from 28 populations, and a total of eight chlorotypes were identified. The presence of definite phylogeographic structure was detected for the species (NST > GST, P < 0.001), and phylogenetic analysis indicated that the eight chlorotypes were clustered into two divergent lineages. They split at approximately 550–690 ka BP, according to coalescence analysis, coincident with the Pleistocene maximum glacial stage in these mountains, which suggests the restriction of these lineages to separate refugia at that time. Spatial analysis of molecular variance likewise divided the sampled populations into two associations, an Altai and eastern Tianshan group (populations 1–17), and a western Tianshan group (populations 18–28). Low levels of genetic diversity and unimodal mismatch distributions were obtained for both of these groups, suggesting postglacial range expansions. During the course of these expansions, mountain ranges surrounding the Dzungarian Basin probably served as migration corridors. In addition, a contact zone was identified in the central Tianshan and eastern Altai Mountains between the two phylogeographic lineages.
    • Guo-Dong LI, Liang-Liang YUE, Hang SUN, Zi-Gang QIAN
      2012, 50 (4): 305–315
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      Phylogeographic studies on alpine plants endemic to the Hengduan Mountains of the southeastern Qinghai–Tibet Plateau are still limited in number. In this study, we used sequence variation of one nuclear gene (ncpGS, which encodes the chloroplastic glutamine synthetase) and in two chloroplast DNA segments to investigate the phylogeographic structure and population demographic history of Cyananthus delavayi, a narrow-range species endemic to this region. We identified eight chlorotypes and 16 nuclear genotypes in a survey of 10 populations sampled throughout the range of the species. The results of both phylogenetic and network analyses suggested that the genealogical relationships of both chlorotypes and nuclear genotypes showed a clear geographical correlation. High total genetic diversity, low levels of within-population diversity, and strong population differentiation (chloroplast DNA: hT= 0.827, hS= 0.087, NST= 0.899, GST= 0.895; nuclear DNA: hT= 0.910, hS= 0.348, NST= 0719, GST= 0.618) were identified. Based on the mismatch distribution analyses, no evidence of recent demographic population expansion was found for this species. Nested clade analyses of both chlorotypes and nuclear genotypes indicated that restricted gene flow resulting from isolation by distance and allopatric fragmentation were likely to have been the major processes that shaped their present-day spatial distribution. Our dating of the genetic divergences between three major geographic lineages suggested that the largest glaciation of the early Quaternary developed in the Qinghai–Tibet Plateau and mountainous isolation may have together led to deep intraspecific vicariance within this species.
    • Zhi-Yun YANG, Ting-Shuang YI, Yue-Zhi PAN, Xun GONG
      2012, 50 (4): 316–324
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      The Hengduan Mountains region is considered to be an important reservoir and a differentiation center for temperate and alpine plants during the Cenozoic. To reveal the effects of extreme topography and climate on an organism's population genetic structure in this region, a phylogeographic study has been carried out for Ligularia vellerea. We sequenced two chloroplast DNA fragments, trnH-psbA and trnL-rpl32, for 157 individuals of 15 populations and a total of 14 haplotypes were identified. These haplotypes clustered into five clades and each of them was mainly distributed in the restricted regions. A strong phylogeographic structure of this species was detected (NST= 0.851, GST= 0.713; NST > GST, P < 0.01). The strong population differentiation in L. vellerea could be attributed to the repeated glacial/interglacial cycles during the Pleistocene, which has been further enhanced by restricted gene flow caused by the complicated topography in the Hengduan Mountains region that formed during the uplift of the Qinghai–Tibet Plateau.
    • Xiao-Hong LI, Jian-Wen SHAO,Chang LU, Xiao-Ping ZHANG, Ying-Xiong QIU
      2012, 50 (4): 325–333
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      Pteroceltis tatarinowii Maxim. (Ulmaceae), one of the most widespread temperate canopy trees in mainland China, is the sole representative of the genus Pteroceltis. To illuminate the biogeographic and demographic history of this temperate tree species, we carried out a survey of chloroplast DNA sequence variation (trnS-trnG and psbA-trnH) within and among 28 populations (284 individuals in total) representing most of the distributional range of the species. Based on a total of 13 haplotypes identified, P. tatarinowii was found to harbor surprisingly high levels of haplotype and nucleotide diversity (hT= 0.71; πT= 2.83 × 10−3), possibly associated with its long evolutionary history and wide-scale geographical distribution. Significant chloroplast DNA population subdivision was detected (GST= 0.898; NST= 0.938), suggesting low levels of recurrent gene flow through seeds among populations and significant phylogeographical structure (NST > GST, P < 0.05). The ancestral haplotypes show clear-cut geographical distribution, and most regions possess a unique set of haplotypes, suggesting multiple potential refugia of the species occurring in montane areas of South China. The haplotype mismatch distributions analysis indicates that populations from North China underwent a spatial northward expansion, which might reflect one of the repeated Pleistocene south-to-north shifts of temperate deciduous forest in North China following cold periods.
    • Jia-Xing AN, Qian WANG, Ji YANG, Jian-Quan LIU
      2012, 50 (4): 334–340
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      Phragmites australis is a cosmopolitan clonal species, but one haplotype from Eurasia has become highly invasive in North America. This article describes an investigation of the phylogeographic composition of 77 populations from China, based on the sequencing of two chloroplast non-coding DNA regions. A total of 11 haplotypes were detected, based on the sequence alignments of two chloroplast DNA fragments from 421 sampled individuals. Six of these haplotypes were completely new, and did not correspond to any of this species’ 27 previously known haplotypes. The invasive haplotype M and haplotypes O and P were shown to occur frequently. Haplotype O is widely distributed across all regions and probably represents the primitive haplotype of this species. In contrast, P is mainly distributed in the humid eastern and northeastern regions of China, whereas M is more frequent in western and northwestern China—arid habitats with low precipitation. Between eastern and northeastern and western and northwestern regions, there was distinct genetic differentiation; the former region has a higher genetic diversity than the latter. The high occurrence of haplotype M in western China suggests that it prefers more arid habitats. These findings shed new light on the native distribution, adaptation, and habitat preference of haplotype M, which invaded North America.
    • Jia-Bin ZOU, Xiao-Li PENG, Long LI, Jian-Quan LIU, Georg MIEHE, Lars OPGENOORTH
      2012, 50 (4): 341–350
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      The aim of the present study was to examine the phylogeographic and evolutionary history of Picea likiangensis, a dominant species of the conifer forests in the eastern declivity of the Qinghai–Tibetan Plateau. We collected 422 individuals from 42 natural populations of three major varieties classified under this species. In conifers, mitochondrial (mt) DNA and chloroplast (cp) DNA dispersed by seeds or pollen experience very different levels of gene flow. To this end, we examined the sequence variation of two mtDNA fragments (nad5 intron 1 and nad1 intron b/c) and three cpDNA fragments (trnL–trnF, trnS–trnG and nadhK/C). We found that cpDNA probably introgressed from P. purpurea into remote populations of P. likiangensis through long-distance dispersal. Multiple refugia seem to have been maintained for P. likiangensis during the Last Glacial Maximum because the cpDNA and mtDNA haplotypes recovered were fixed in the different regions. Postglacial expansions were only detected at the distributional edges of this species where a single cpDNA or mtDNA haplotype was fixed in adjacent populations. However, genetic imprints of postglacial expansions from these two sets of markers were different in the western and southeastern regions, which may result from the long-distance dispersal of the cpDNA, as well as its fast lineage sorting during intraspecific divergences. Analysis of molecular variance further suggested that genetic differentiation between the three varieties is higher at cpDNA markers than at mtDNA markers, which supports the previous viewpoint that cpDNA markers with a high rate of gene flow may be more effective in delimitating closely related taxa. Together, the results of the present study highlight the evolutionary complexity of a widely distributed species owing to interactions among local and edge expansion, long-distance dispersal, and intraspecific divergences at two sets of DNA genomes with different rates of gene flow.
    • Zhong-Hu LI, Jian CHEN, Gui-Fang ZHAO, Yu-Peng GUO, Yi-Xuan KOU,Ya-Zheng MA, Gang WANG, Xiao-Fei MA
      2012, 50 (4): 351–361
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      Past geological and climatic events have promoted intraspecific divergence and range shifts in numerous plant species. This is particularly true for temperate species in climate-sensitive regions. Few previous studies have examined whether such genetic footprints were also shaped in desert plants, which can survive in arid habitats and might be “static” under the past climatic oscillations. We therefore studied the phylogeographical history of Reaumuria soongarica, a shrub species that is widely distributed across the deserts of western China. We sequenced chloroplast DNA (cpDNA) fragments of 27 natural populations across western China. Eight cpDNA haplotypes were identified, which clustered into three clades. The clades were located in the western (clade II) or eastern regions (clades I and III) of western China. Analysis of molecular variance also supported this major partitioning (∼67%) of the cpDNA variation between regions. However, within each region, genetic differentiation was low (29%–37%) and a single dominant haplotype was fixed; this indicated past regional range expansion. The deep divergence and regional range expansions of this species may have corresponded to the most recent uplift of the Qinghai–Tibet Plateau and the development of desert ecosystems during the last glacial age in western China. This is the first study to show that the evolutionary history of plants in desert habitats has been seriously affected by past geological and climatic change.
    • Yong LI, Hai-Fei YAN, Xue-Jun GE
      2012, 50 (4): 362–373
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      The phylogeography of common and widespread species can help us to understand the history of local flora and vegetation. Here, we study the semi-evergreen shrub Rhododendron simsii Planch., which is found in most areas of current evergreen broad leaved forest in China. Two noncoding chloroplast DNA (cpDNA) regions (rpl20-rps12 and trnL-F) and three amplified fragment length polymorphism (AFLP) primer sets (E-AAC/M-CTA, E-AGC/M-CTA and E-AGG/M-CAT) were used to examine the phylogeographic pattern in relation to past (last glacial maximum) and present distributions based on ecological niche modeling. The cpDNA data revealed four phylogeographic groups (East, South, West, and North groups) corresponding to geographic regions. Molecular dating suggests that lineage diversification within species likely occurred during the mid-to-late Pleistocene. In contrast, the four main cpDNA phylogeographic groups were not supported by the AFLP dataset. The highest likelihood of the AFLP data was obtained when samples were clustered into three groups (K= 3). However, these groupings did not correspond to separate geographic regions supported by cpDNA data. Both mismatch distribution analysis and environmental niche modeling (ENM) indicated that multiple glacial refugia were maintained across the range of Rhododendron simsii during the last glacial maximum, contrary to the previous hypothesis that subtropical broad leaved evergreen forests were forced to retreat southward as far as 25° N. The discordance between the patterns revealed by cpDNA and AFLP data indicate that localized postglacial range expansions may facilitate extensive gene flow between the major glacial refugia.
    • Shi-Chao CHEN, Li ZHANG, Jie ZENG, Fei SHI, Hong YANG, Yun-Rui MAO, Cheng-Xin FU
      2012, 50 (4): 374–385
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      The monotypic genus Platycarya (Juglandaceae) is one of the most widespread temperate tree species in East Asia. In this research, we implemented a phylogeographical study using chloroplast DNA (cpDNA) (psbA-trnH and atpB-rbcL intergenic spacer) sequences on Platycarya strobilacea, in order to identify the locations of the species’ main refugia and migration routes. A total of 180 individuals of P. stobilacea from 27 populations from China and Jeju Island (Korea) were collected. The results revealed that P. strobilacea had 35 haplotypes for the two intergenic spacers and high genetic diversity (hT= 0.926). This surprisingly high diversity of haplotypes indicates its long evolutionary history, which is in agreement with previous phylogenetic analyses and fossil records. Significant cpDNA population subdivision was detected (GST= 0.720; NST= 0.862), suggesting low levels of recurrent gene flow through seeds among populations and significant phylogeographical structure (NST > GST, P < 0.05). The construction of phylogenetic relationships of the 35 chlorotypes detected four major cpDNA clades. Divergence dating analyses using BEAST suggest that the divergence of the major cpDNA clades occurred before the Miocene. Demographic analysis indicated that the Eastern clade underwent localized demographic expansions. The molecular phylogenetic data, together with the geographic distribution of the haplotypes, suggest the existence of multiple glacial refugia in most of its current range in China through Quaternary climatic oscillations.
Song Ge
Jun Wen
Impact Factor
JCR 2022 IF ranking: 60/238 (Plant Sciences, top 25%, Q2 quartile)
Journal Abbreviation: J Syst Evol
ISSN: 1674-4918 (Print)
1759-6831 (Online)
CN: 11-5779/Q
Frequency: Bi-monthly




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