- Research article
- Open Access
Genetic and geographical structure of boreal plants in their southern range: phylogeography of Hippuris vulgaris in China
© Lu et al. 2016
- Received: 7 October 2015
- Accepted: 28 January 2016
- Published: 9 February 2016
Our current understanding of the evolutionary history of boreal and arctic-alpine plants in their southern range in Asia remains relatively poor. Using three cpDNA non-coding regions and nine nuclear microsatellite (nSSR) loci, we examine the phylogeographic pattern in a broad geographic sampling of the boreal plant Hippuris vulgaris to infer its dispersal and diversification in China. In addition, the species distributions at the Last Glacial Maximum (LGM) and at present were predicted using ecological niche modeling (ENM).
The cpDNA results revealed two distinct lineages, A and B. A is restricted to Northeast China; B is distributed in Northwest China, the Qinghai-Tibet Plateau (QTP) and North and Northeast (NNE) China; and A and B diverged ca. 1.36 Ma. The nSSR data revealed two genetic clusters corresponding to the two cpDNA lineages and nonreciprocal hybridization with lineage A as the maternal lineage in Northeast China. Cluster B further divided into three subclusters: I, mainly in NNE China and the northeastern border of the QTP; II, in Northwest China and the QTP; and III, on the QTP. ENM predicted a marked range shift on the QTP at the LGM, retreating from the platform to the northeast and southeast edges.
Hippuris vulgaris probably diverged into lineages A and B in high latitudes and then immigrated into Northeast China and Northwest China, respectively. Lineage A persisted and diversified in Northeast China. Lineage B reached the QTP during the mid-Pleistocene, diversified in that region due to the influence of climatic oscillations, migrated into Northeast China and subsequently hybridized with lineage A. Our findings give empirical evidence that boreal plants display complex evolutionary history in their southern range in Asia and provide new insights into the evolution of boreal and arctic-alpine plants.
- Boreal plants
- Chloroplast DNA
- Ecological niche modeling
- Hippuris vulgaris
Climatic oscillations in the Quaternary have greatly affected the distribution and abundance of boreal and arctic species . These species have undergone major range shifts with the advances and retreats of ice sheets. In the past two decades, numerous studies have focused on plant species in boreal regions and/or arctic latitudes and southern mountain ranges, and different phylogeographic patterns amongst plants have been revealed, especially in Europe and North America [2–5]. Some of these studies included samples from mountains in Central Asia have revealed that Central Asia is an important refugium for boreal and arctic plants and colonization from Central Asia to Europe or to Beringia are conceivable [6–10]. However, colonization routes of these species between Central Asia and mountains in low latitudes in Asia need to be further explored. At present, our understanding of the southern range dynamics of boreal and arctic-alpine plants in Asia is based mostly on data from Japan [11–13]. Phylogeographic studies with a broader geographic sampling in Asia are necessary to better elucidate evolutionary histories of boreal and arctic-alpine plants.
China provides suitable habitats for many boreal and arctic-alpine plant species in their southern range, including the Qinghai-Tibetan Plateau (QTP) and mountain ranges in Northwest China and Northeast China . Two putative routes have been suggested for the migration of the flora between the QTP and the arctic regions: one is the “Central Asiatic Highland Corridor” pathway via mountain ranges in Northwest China , and another is the “Himalayan-Hengduan Mountain-Qinling-Northeast China” route . We thus hypothesized that similar colonization routes might also be present in a single species of this plant group. In addition, the QTP is considered a center of the development and differentiation of the elements from boreal or Arctic-Tertiary flora since the late Tertiary and Quaternary glacial periods . Similarly, infra-specific lineage divergence in boreal and arctic-alpine plants might also occur in this region.
To infer refugial areas and colonization routes of boreal and arctic-alpine plants in China, we should conduct phylogeographic studies on species with a widespread range covering the QTP and mountains in northeast and northwest China. In this study, we focused on Hippuris vulgaris (Plantaginaceae), an aquatic plant of circumboreal distribution. China is the southern range of this species in Asia, and H. vulgaris is mainly distributed in the north, northeast, northwest and southwest of China . The plant is rhizomatous perennial and often grows in fresh water at the edges of ponds, lakes and rivers. A recent chloroplast DNA (cpDNA) phylogeography of H. vulgaris in the QTP and adjacent areas revealed a mid-to-late Pleistocene split of two lineages on the QTP and possible colonization between the QTP and Northwest China , whereas no specific refugia areas were deduced and no samples from Northeast China were included. We hypothesized that colonization between the QTP and Northeast China was likely existed in H. vulgaris. In the present study, we used both cpDNA sequences and nuclear microsatellite (nSSR) data to examine the phylogeographic pattern of H. vulgaris based on a large-scale sampling covering its distribution range in China. In addition, we inferred the glacial range dynamics of H. vulgaris by using ecological niche modeling (ENM; ). Our aims were to (1) test whether lineage divergence on the QTP was detected by both cpDNA and nSSR, and (2) deduced potential refugia and putative colonization routes of H. vulgaris in China. Investigating these questions was conducive to (3) elucidating the evolutionary history of H. vulgaris in its southern range in Asia.
A total of 637 individuals were collected at 91 sites throughout the distribution range of H. vulgaris in China, including Northwest China, the QTP, and North and Northeast (NNE) China (Additional file 1). At each site, 1–16 individuals were sampled at intervals of at least 5 m according to the population size. The leaf material of each individual was collected and immediately stored in silica gel. Voucher specimens were deposited in the herbarium of Wuhan University (WH).
DNA extraction, amplification and sequencing
Total genomic DNA was extracted from silica-dried leaves using the DNA secure Plant Kit (Tiangen Biotech, Beijing, China). Six cpDNA non-coding regions were examined in preliminary experiment in 2012 and three regions, trnH-psbA , trnQ-rps16 and rps16-trnK , were chosen due to their high polymorphism (Additional file 2). Polymerase chain reaction (PCR) was performed in a volume of 25 μL containing 10–30 ng of genomic DNA, 0.1 μM of each primer, 0.2 mM of each dNTP, 2 mM MgCl2 and 0.6 U of ExTaq DNA polymerase (TaKaRa, Dalian, China) under the following conditions: 3 min at 95 °C, followed by 35 cycles of 30 s at 95 °C, 30 s at 55 °C, and 90 s at 72 °C, and then a final 5 min extension at 72 °C. Amplifications were conducted in a Veriti 96-Well Thermal Cycler (Applied Biosystems, Foster City, USA). The PCR products were purified and sequenced by the Beijing Genomic Institute in Wuhan, China.
Microsatellite loci development and genotyping
We developed nSSR primers using the microsatellite-enriched library method. Detailed methods and processes followed Wu et al. . A total of nine nSSR loci were developed for subsequent analysis (Additional file 3). Microsatellites were amplified under the following conditions: 3 min at 95 °C; 35 cycles of 30 s at 95 °C, 30 s at 49–57 °C (Additional file 3), and 1 min at 72 °C; and a final extension at 72 °C for 5 min. PCR products were analyzed on an ABI 3730XL, and genotyping was performed using GeneMapper version 4.0 software (Applied Biosystems).
Population genetic structure analyses
All cpDNA sequences were aligned using the program MAFFT 6.7 . The three chloroplast fragments were concatenated for subsequent analyses. Identical sequences were collapsed into a single haplotype using DNASP 5.10 , and all sequences of different haplotypes were deposited in GenBank (Accession Nos. KT921227- KT921258). A statistical parsimony network was constructed using TCS 1.21 , treating sequence gaps as the fifth character state. In the network analysis, gaps of two or more base pairs were re-coded as single-base-pair indels.
Regarding the nSSR data, genetically distinct clusters of 91 populations were identified using an individual-based assignment approach as implemented in STRUCTURE 2.3.4 . Ten independent runs were performed for each K value (K = 1 to 16) with a burn-in period of 20,000 iterations and 100,000 Markov chain Monte Carlo (MCMC) iterations under the admixture model. The best-fit number of clusters was determined based on the ∆K method . The geographical distribution of different cpDNA haplotypes and nSSR clusters identified was mapped using ArcGIS 9.0 (Esri, Redlands, CA, USA). For both cpDNA and nSSR data, analyses of molecular variance (AMOVA) were used to partition genetic variation among and within populations, as implemented in ARLEQUIN 3.1 . The individuals with the same nSSR genotype were removed and only one was kept within a population in genetic analyses.
Phylogenetic reconstruction and divergence time estimation
The phylogenetic relationships of cpDNA haplotypes were inferred using maximum likelihood (ML) analysis implemented in GARLI 0.951 , starting from random trees and using 10,000,000 generations per search. The ML bootstrap support was estimated from 1000 bootstrap replicates in GARLI. Bayesian inference (BI) implemented in MrBayes 3.1.2  was also used for phylogenetic reconstruction. Two independent MCMC analysis runs were conducted simultaneously, beginning with a random tree, with each run including four chains (one cold and three hot). Two million generations were run, with sampling at every 1,000 generations. Chain convergence was checked using Tracer 1.5 , and the first 25 % of samples were discarded as burn-in. The K81uf + I substitution model for the ML and BI analyses was identified using the Akaike information criterion (AIC) implemented in ModelTest 3.7 . The divergence times of cpDNA lineages were estimated by using a Bayesian method implemented in BEAST 1.4.7 . An evolutionary rate of 1.52 × 10−9 s/s/y  for the three combined cpDNA non-coding regions was used to estimate divergence time under an uncorrelated lognormal relaxed clock model. MCMC analysis of 50,000,000 generations was implemented, in which every 1,000 generations were sampled. The first 10 % of generations were discarded as burn-in, and the parameters were checked using Tracer 1.5.
Regarding the cpDNA data, we examined pairwise mismatch distributions to detect historical demographic expansions using ARLEQUIN. The sum of squared deviations (SSD) and Harpending’s raggedness index (Rag)  were used to test the goodness of fit under a sudden-expansion model. Their significances were tested using a parametric bootstrap approach with 1,000 replicates . We also performed two powerful tests, Fu’s F S test  and the R 2 test , to detect potential population growth using DNASP.
Present and past distribution modeling
ENM was used to predict the suitable past (Last Glacial Maximum, LGM) and present climate envelopes for each lineage (see results), as implemented in MAXENT 3.3.3 k [20, 40]. In addition to the 91 sites in this study (Additional file 1), 47 sites from Chen et al.  and 68 collection records from the Chinese Virtual Herbarium (www.cvh.org.cn) were included. Based on this total of 206 records, we obtained an environmental data set comprising 19 BioClim variables and altitudes from the WORLDCLIM database with resolutions of 2.5’ (; www.worldclim.org). We examined pairwise correlations among the 20 variables and retained seven environmental variables (annual mean temperature, temperature seasonality, temperature annual range, mean temperature of warmest quarter and coldest quarter, precipitation of warmest quarter and coldest quarter) with pairwise Pearson correlation coefficients of r < 0.7 to minimize biased fitting of niche models. A current distribution model was developed using these seven bioclimatic data layers. This model was then projected onto the LGM dataset simulated by the Community Climate System Model v3.0 . We used the default parameters of MAXENT to construct ENMs. The accuracy of each model prediction was evaluated using the area under the (receiver operating characteristic) curve (AUC).
Chloroplast DNA haplotype network
Phylogenetic lineages and divergence time
The trees generated using ML and BI analyses showed the same topology, in which two reciprocally monophyletic lineages (A and B) were recovered with robust support (Fig. 1b). These two lineages corresponded to the two groups in the haplotype network. The divergence time of the two lineages was estimated at 1.36 Ma ago (Ma) (with a 95 % highest posterior density [HPD] interval of 0.66 - 2.52 Ma), which yields time estimates in the early Pleistocene. The diversification of lineages A and B was estimated at 0.65 Ma (95 % HPD: 0.22 - 1.33 Ma) and 0.53 Ma (95 % HPD: 0.17 - 1.22 Ma), respectively (Fig. 1b), both of which are in the mid-Pleistocene.
Population genetic structure
The STRUCTURE analysis using SSR data suggested K = 2 as the optimal number of genetic clusters based on the calculation of ΔK (Additional file 4). We defined these two clusters as A and B. All individuals of 18 and 63 populations were assigned to cluster A and B with a posterior probability higher than 0.95 (Additional file 5) and had cpDNA lineages A and B, respectively (Fig. 2c, d). Most or all individuals of nine populations were admixed with a probability range from 0.326 to 0.890 (Additional file 5) and had cpDNA lineage A (Fig. 2c). In population ARQ1, two individuals with admixed assignment had cpDNA lineage A, and other individuals with cluster B assignment had cpDNA lineage B (Additional file 5). All of the results suggested that hybridization occurred between lineage A and B and that hybrids were produced only when lineage A was the ovulate parent. Further STRUCTURE analysis was also performed for cluster A and cluster B, and the optimal solution was K = 2 and K = 3, respectively (Additional file 4). In cluster A, all individuals were admixed and no subclusters were identified (Additional file 5). In cluster B, most individuals were assigned to three subclusters with high posterior probability (Additional file 5). These three subclusters had different geographic distributions: subcluster I mainly occurred in NNE China and Northeast QTP edge, subcluster II was mostly found in Northwest China and the QTP, and subcluster III was restricted to the QTP (Fig. 2d).
Analyses of molecular variance based on cpDNA and nSSR data for populations of Hippuris vulgaris
Source of variation
Percentage of total variance (%)
Percentage of total variance (%)
Among populations within lineages
Among populations within regions
Summary of mismatch distribution parameters and neutrality test for two lineages of Hippuris vulgaris
Fu’s F S
Present and past (LGM) distribution of lineages
Both cpDNA and nSSR results show that H. vulgaris in China is composed of two distinct lineages A and B with different geographic distributions. The distribution ranges of three other species in the genus Hippuris are to the north of 53° north latitude, which are in the north of the range of H. vulgaris [43, 44]. In addition, the fossil records of H. vulgaris, e.g., one of Plio-Pleistocene age from North Greenland  and another of middle and upper Pleistocene from central England , were also found in the north area of its present distribution. Both species distribution and fossil record suggested that the ancestral range of H. vulgaris was in the north of its present range and probably to the north of 53° north latitude. Therefore, lineages A and B had likely split in high latitudes before they migrated into China. The occurrence of different infra-specific lineages in high latitudes of Asia has been revealed in some arctic-alpine plants [3, 5, 6, 8, 9, 47]. Our molecular dating indicates that the divergence of lineages A and B occurred during the early Pleistocene (ca. 1.36 Ma), a period displaying minor glacial/interglacial variability before the mid-Pleistocene revolution followed with higher-amplitude fluctuations , suggesting that the latitudinal range shifts during the early Pleistocene may not have been sufficient to push H. vulgaris southwards into China. The mid-Pleistocene stem ages of lineage A and lineage B (Fig. 1b) also suggest that the two lineages migrated into China driven by the mid-Pleistocene glaciations and thereafter diversified separately. This scenario needs to be tested by further studies including samples from high latitudes of Asia.
Lineage A is restricted to Northeast China, indicating its immigration southwards into this region. The stem age of lineage A in the mid-Pleistocene (ca. 0.65 Ma) and the occurrence of its potential distribution in the lowland areas of Northeast China at the LGM (Fig. 3b) suggest that long-standing populations have persisted in Northeast China for several glacial/interglacial cycles. For lineage B, the migration route is more complex. Because the development of a wide arid belt or dryland in northern China and the Republic of Mongolia since ca. 2.6 Ma [49, 50] probably acted as a strong physical barrier for aquatic plant dispersal between Northeast China and Northwest China, lineage B should immigrate into China either from Northeast China or from Northwest China. Direct dispersal between the two regions was unlikely, therefore, lineage B reached its present distribution by dispersal either from Northeast China via the QTP to Northwest China or via the reverse route. The former route seems likely because NNE China had the largest number of haplotypes (Fig. 2b), whereas the latter route is supported by the fact that only subcluster I was found in NNE China (Fig. 2d). Combined with the exclusive occupation of the north range of Northeast China by lineage A (Fig. 2a) and the occurrence of inter-lineage hybrids only in Northeast China (Fig. 2c), we considered it more likely that lineage B immigrated southwards into Northwest China, dispersed to the QTP and subsequently migrated into NNE China (Fig. 2d).
The dispersal between highlands in Northwest China and the QTP via the “Central Asiatic Highland Corridor” pathway has been suggested  for the migration of the flora between the QTP and the arctic regions. This dispersal pathway was also suggested by Wen et al.  and verified through the results of a few recent phylogenetic and phylogeographic studies: the same or closely related lineages were present in the two regions [8, 52–54]. As for H. vulgaris, its dispersal between Northwest China and the QTP was supported by a shared cpDNA haplotype (Fig. 2b; ) and the same genetic subcluster II (Fig. 2d) present in the two regions. This colonization was also in accordance with the migratory route of waterbirds in China [55, 56], which is an important vector for long-distance dispersal of aquatic plants [57, 58]. Furthermore, the fact that H. vulgaris is common in the diet of waterbirds at northern latitudes  indicates the possibility of long-distance dispersal by waterbirds in H. vulgaris. The dispersal between the QTP and Northeast China likely occurred through the “Himalayan-Hengduan Mountain-Qinling-Northeast China” route suggested by Wang , based on the geographic distribution of some plants. However, for H. vulgaris, another route between Northeast QTP edge and Northeast China seems more likely because the populations from Northeast QTP edge were assigned to genetic subcluster I, the same subcluster as populations from NNE China (Fig. 2d). This route is consistent with the dispersal pathway of a subspecies of sea buckthorn .
The QTP has biogeographic significance for alpine plant evolution . Based on evidence from phylogenetic studies on several taxa, Wen et al.  suggested a pattern of Central Asian origin with subsequent diversification on the QTP. This pattern is suitable for lineage B of H. vulgaris. The stem age of lineage B in the mid-Pleistocene (ca. 0.53 Ma) is similar to the result of Chen et al.  (ca. 0.48 Ma), estimated based on another cpDNA dataset collected from samples on the QTP, suggesting that H. vulgaris reached the QTP during the mid-Pleistocene. Two lineages were revealed on the QTP in Chen et al. , whereas no cpDNA lineage divergence except three private haplotypes was detected in the present study (Figs. 2b and 3), likely resulting from the use of different fragments. When nSSR data were considered, three subclusters were identified on the QTP: subcluster I in northeast edge, subcluster II from west to east, and subcluster III from middle to east (Fig. 2d). Chen et al. found that two cpDNA lineages was overlapped distribution and co-occurred in some populations due to repeated range expansions . This conclusion is confirmed by our nSSR data because the same pattern was also revealed in our populations of subclusters II and III (Fig. 2d) and the sampling of Chen et al.  did not cover Northeast QTP edge. In addition, we tried to use ENM to infer potential glacial refugia of H. vulgaris based on BioClim variables. The distributions of aquatic plants species are correlated with climatic factors [61–63] and occurrences of different genetic lineages are associated with environmental dissimilarity or latitudinal difference in some widespread species [64, 65], indicating that eco-climatological niche modeling based on BioClim variables is applicable for aquatic plants. Based on the prediction of ENM, a marked range shift occurred in H. vulgaris at the LGM, retreating from the platform to the northeast edge and southeast edge (Fig. 3c, d). This scenario and the locations of potential glacial refugia have been suggested by many phylogeographic studies on the QTP [66, 67]. The lineage divergence of H. vulgaris on the QTP was likely promoted by repeated climatic oscillations during mid-late Pleistocene.
Our study reveals that Hippuris vulgaris is highly structured genetically and geographically in China, with signs of immigration, dispersal, diversification and hybridization. This study provides empirical evidence that boreal plants display complex evolutionary history in their southern range in Asia. Comparative studies on other boreal and arctic-alpine plants would be valuable for better understanding the colonization and diversification in their southern range in Asia.
The data set supporting the results of this article is included within the article and its additional files. The 26 cpDNA sequences supporting the results of this article are available in the National Center for Biotechnology Information (GenBank) under accession numbers KT921227-KT921258, http://www.ncbi.nlm.nih.gov/Genbank/. Moreover, the nSSR data and datasets for ecological niche modeling are deposited in LabArchives (http://www.labarchives.com/bmc) and are available via the DOI http://dx.doi.org/10.6070/H4K64G3F.
This study was supported by grants from the National Natural Science Foundation of China to Xinwei Xu (31070190 and 31270265) and Dan Yu (30930011). We thank the members of Dan Yu’s group for their advice and field assistance.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Hewitt GM. Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc B. 2004;359:183–95.PubMed CentralView ArticlePubMedGoogle Scholar
- Abbott RJ, Brochmann C. History and evolution of the arctic flora: in the footsteps of Eric Hultén. Mol Ecol. 2003;12:299–313.View ArticlePubMedGoogle Scholar
- Schönswetter P, Popp M, Brochmann C. Central Asian origin of and strong genetic differentiation among populations of the rare and disjunct Carex atrofusca (Cyperaceae) in the Alps. J Biogeogr. 2006;33:948–56.View ArticleGoogle Scholar
- Wróblewska A. The role of disjunction and postglacial population expansion on phylogeographical history and genetic diversity of the circumboreal plant Chamaedaphne calyculata. Biol J Linn Soc. 2012;105:761–75.View ArticleGoogle Scholar
- Eidesen PB, Ehrich D, Bakkestuen V, Alsos IG, Gilg O, Taberlet P, et al. Genetic roadmap of the Arctic: plant dispersal highways, traffic barriers and capitals of diversity. New Phytol. 2013;200:898–910.View ArticlePubMedGoogle Scholar
- Schönswetter P, Popp M, Brochmann C. Rare arctic-alpine plants of the European Alps have different immigration histories: the snow bed species Minuartia biflora and Ranunculus pygmaeus. Mol Ecol. 2006;15:709–20.View ArticlePubMedGoogle Scholar
- Skrede I, Eidesen PB, Portela RP, Brochmann C. Refugia, differentiation and postglacial migration in arctic-alpine Eurasia, exemplified by the mountain avens (Dryas octopetala L.). Mol Ecol. 2006;15:1827–40.View ArticlePubMedGoogle Scholar
- Allen GA, Marr KL, McCormick LJ, Hebda RJ. The impact of Pleistocene climate change on an ancient arctic-alpine plant: multiple lineages of disparate history in Oxyria digyna. Ecol Evol. 2012;2:649–65.PubMed CentralView ArticlePubMedGoogle Scholar
- Winkler M, Tribsch A, Schneeweiss GM, Brodbeck S, Gugerli F, Holderegger R, et al. Tales of the unexpected: Phylogeography of the arctic-alpine model plant Saxifraga oppositifolia (Saxifragaceae) revisited. Mol Ecol. 2012;21:4618–30.View ArticlePubMedGoogle Scholar
- Allen GA, Marr KL, McCormick LJ, Hebda RJ. Geographical origins, migration patterns and refugia of Sibbaldia procumbens, an arctic-alpine plant with a fragmented range. J Biogeogr. 2015;42:1665–76.View ArticleGoogle Scholar
- Ikeda H, Senni K, Fujii N, Setoguchi H. Survival and genetic divergence of an arctic-alpine plant, Diapensia lapponica subsp obovata (Fr. Schm.) Hultén (Diapensiaceae), in the high mountains of central Japan during climatic oscillations. Plant Syst Evol. 2008;272:197–210.View ArticleGoogle Scholar
- Ikeda H, Senni K, Fujii N, Setoguchi H. High mountains of the Japanese archipelago as refugia for arctic-alpine plants: phylogeography of Loiseleuria procumbens (L.) Desvaux (Ericaceae). Biol J Linn Soc. 2009;97:403–12.View ArticleGoogle Scholar
- Ikeda H, Yoneta Y, Higashi H, Eidesen PB, Barkalov V, Yakubov V, et al. Persistent history of the bird-dispersed arctic-alpine plant Vaccinium vitis-idaea L. (Ericaceae) in Japan. J Plant Res. 2015;128:437–44.View ArticlePubMedGoogle Scholar
- Wu ZY, Zhou ZK, Sun H, Li DZ, Peng H. The Areal-Types of Seed Plants and Their Origin and Differentiation. Kunming: Yunnan Science and Technology Press; 2006.Google Scholar
- Ohba H. The Alpine Flora of the Nepal Himalayas: An Introductory Note. Tokyo: University of Tokyo Press; 1988.Google Scholar
- Wang WT. On some distribution patterns and some migration routes found in the eastern Asiatic region. Acta Phytotaxon Sin. 1992;30:1–24.Google Scholar
- Sun H. Evolution of arctic-tertiary flora in Himalayan-Hengduan mountains. Acta Bot Yunnan. 2002;24:671–88.Google Scholar
- Chen JR, Funston AM. Hippuridaceae. In: Wu ZY, Raven PH, editors. Flora of China, vol. 13. Beijing: Science Press and St. Louis: Missouri Botanical Garden Press; 2007. p. 433.Google Scholar
- Chen JM, Du ZY, Sun SS, Gituru RW, Wang QF. Chloroplast DNA phylogeography reveals repeated range expansion in a widespread aquatic herb Hippuris vulgaris in the Qinghai-Tibetan Plateau and adjacent areas. Plos One. 2013;8, e60948.PubMed CentralView ArticlePubMedGoogle Scholar
- Phillips SJ, Anderson RP, Schapire RE. Maximum entropy modeling of species geographic distributions. Ecol Model. 2006;190:231–59.View ArticleGoogle Scholar
- Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, et al. The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot. 2005;92:142–66.View ArticlePubMedGoogle Scholar
- Shaw J, Lickey EB, Schilling EE, Small RL. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot. 2007;94:275–88.View ArticlePubMedGoogle Scholar
- Wu ZG, Yu D, Xu XW. Development of microsatellite markers in the hexaploid aquatic macrophyte, Myriophyllum spicatum (Haloragaceae). Appl Plant Sci. 2013;2, e1200230.Google Scholar
- Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 2008;9:286–98.View ArticlePubMedGoogle Scholar
- Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25:1451–2.View ArticlePubMedGoogle Scholar
- Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Mol Ecol. 2000;9:1657–9.View ArticlePubMedGoogle Scholar
- Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–59.PubMed CentralPubMedGoogle Scholar
- Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14:2611–20.View ArticlePubMedGoogle Scholar
- Excoffier L, Laval G, Schneider S. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform Online. 2005;1:47–50.PubMed CentralGoogle Scholar
- Zwickl DJ. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas at Austin; 2006.Google Scholar
- Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.View ArticlePubMedGoogle Scholar
- Rambaut A, Drummond AJ. Tracer: MCMC trace analysis tool, version 1.5. 2007. http://tree.bio.ed.ac.uk/software/tracer. Accessed 19 May 2014.
- Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14:817–8.View ArticlePubMedGoogle Scholar
- Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214.PubMed CentralView ArticlePubMedGoogle Scholar
- Yamane K, Yano K, Kawahara T. Pattern and rate of indel evolution inferred from whole chloroplast intergenic regions in sugarcane, maize and rice. DNA Res. 2006;13:197–204.View ArticlePubMedGoogle Scholar
- Harpending HC. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol. 1994;66:591–600.PubMedGoogle Scholar
- Schneider S, Excoffier L. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates very among sites: application to human mitochondrial DNA. Genetics. 1999;152:1079–89.PubMed CentralPubMedGoogle Scholar
- Fu YX. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997;147:915–25.PubMed CentralPubMedGoogle Scholar
- Ramos-Onsins SE, Rozas J. Statistical properties of new neutrality tests against population growth. Mol Biol Evol. 2002;19:2092–100.View ArticlePubMedGoogle Scholar
- Phillips SJ, Dudik M. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography. 2008;31:161–75.View ArticleGoogle Scholar
- Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25:1965–78.View ArticleGoogle Scholar
- Collins WD, Bitz CM, Blackmon ML, Bonan GB, Bretherton CS, Carton JA, et al. The community climate system model version 3 (CCSM3). J Clim. 2006;19:2122–43.View ArticleGoogle Scholar
- Elven R, Murray DF, Solstad H. Hippuris (Plantaginaceae). In: Flora of North America, Provisional Publication. Flora of North America Association. 2012. http://floranorthamerica.org/files/Hippuris03h.CH for Prov Pub.pdf. Accessed 15 May 2015.
- Secretariat GBIF. GBIF Backbone Taxonomy. 2013. http://www.gbif.org/species/3039572. Accessed 29 November 2015.
- Bennike L, Bӧcher J. Forest-tundra neighbouring the North Pole: plant and insect remains from the Plio-Pleistocene Kap Køzrbenhavn Formation, North Greenland. Arctic. 1990;43:331–8.View ArticleGoogle Scholar
- Kelly MR. Floras of middle and upper Pleistocene age from Brandon, Warwickshire. Phil Trans R Soc B. 1968;254:401–15.View ArticleGoogle Scholar
- Skrede I, Borgen L, Brochmann C. Genetic structuring in three closely related circumpolar plant species: AFLP versus microsatellite markers and high-arctic versus arctic-alpine distributions. Heredity. 2009;102:293–302.View ArticlePubMedGoogle Scholar
- Becquey S, Gersonde R. Past hydrographic and climatic changes in the Subantarctic Zone of the South Atlantic - The Pleistocene record from ODP Site 1090. Palaeogeogr Palaeocl. 2002;182:221–39.View ArticleGoogle Scholar
- Lu H, Wang X, Li L. Aeolian sediment evidence that global cooling has driven late Cenozoic stepwise aridification in central Asia. In: Clift PD, Tada R, Zheng H, editors. Monsoon Evolution and Tectonics - Climate Linkage in Asia, vol. 243. London: Special Publications, Geological Society; 2010. p. 29–44.Google Scholar
- Cai MT, Fang XM, Wu FL, Miao YF, Appel E. Pliocene-Pleistocene stepwise drying of Central Asia: evidence from paleomagnetism and sporopollen record of the deep borehole SG-3 in the western Qaidam Basin, NE Tibetan Plateau. Global Planet Change. 2012;94–95:72–81.View ArticleGoogle Scholar
- Wen J, Zhang JQ, Nie ZL, Zhong Y, Sun H. Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau. Front Genet. 2014;5:4.PubMed CentralPubMedGoogle Scholar
- Yang FS, Li YF, Ding X, Wang XQ. Extensive population expansion of Pedicularis longiflora (Orobanchaceae) on the Qinghai-Tibetan Plateau and its correlation with the Quaternary climate change. Mol Ecol. 2008;17:5135–45.View ArticlePubMedGoogle Scholar
- Li GD, Kim C, Zha HG, Zhou Z, Nie ZL, Sun H. Molecular phylogeny and biogeography of the arctic-alpine genus Lagotis (Plantaginaceae). Taxon. 2014;63:103–15.View ArticleGoogle Scholar
- Wang Q, Liu JQ, Allen GA, Ma Y, Yue W, Marr KL, et al. Arctic plant origins and early formation of circumarctic distributions: a case study of the mountain sorrel, Oxyria digyna. New Phytol. 2016;209:343–53.View ArticlePubMedGoogle Scholar
- Sibley CG, Monroe BL. Distribution and Taxonomy of Birds of the World. New Haven: Yale University Press; 1990.Google Scholar
- MacKinnon JR, Sha M, Cheung C, Carey G, Zhu X, Melville D. A Biodiversity Review of China. WWF International: Hong Kong; 1996.Google Scholar
- Clausen P, Nolet BA, Fox AD, Klaassen M. Long-distance endozoochorous dispersal of submerged macrophyte seeds by migratory waterbirds in northern Europe-a critical review of possibilities and limitations. Acta Oecol. 2002;23:191–203.View ArticleGoogle Scholar
- Figuerola J, Green AJ. Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Freshwater Biol. 2002;47:483–94.View ArticleGoogle Scholar
- Dessborn L, Brochet AL, Elmberg J, Legagneux P, Gauthier-Clerc M, Guillemain M. Geographical and temporal patterns in the diet of pintail Anas acuta, wigeon Anas penelope, mallard Anas platyrhynchos and teal Anas crecca in the Western Palearctic. Eur J Wildl Res. 2011;57:1119–29.View ArticleGoogle Scholar
- Jia DR, Abbott RJ, Liu TL, Mao KS, Bartish IV, Liu JQ. Out of the Qinghai-Tibet Plateau: evidence for the origin and dispersal of Eurasian temperate plants from a phylogeographic study of Hippophaë rhamnoides (Elaeagnaceae). New Phytol. 2012;194:1123–33.View ArticlePubMedGoogle Scholar
- Stuckey RL. Phytogeographical outline of aquatic and wetland angiosperms in continental eastern North America. Aquat Bot. 1993;44:259–301.View ArticleGoogle Scholar
- Jacobs SWL, Wilson KL. A biogeographical analysis of the freshwater plants of Australasia. Aust Syst Bot. 1996;9:169–83.View ArticleGoogle Scholar
- Chambers PA, Lacoul P, Murphy KJ, Thomaz SM. Global diversity of aquatic macrophytes in freshwater. Hydrobiologia. 2008;595:9–26.View ArticleGoogle Scholar
- Zhu JN, Yu D, Xu XW. The phylogeographic structure of Hydrilla verticillata (Hydrocharitaceae) in China and its implications for the biogeographic history of this worldwide-distributed submerged macrophyte. BMC Evol Biol. 2015;15:95.PubMed CentralView ArticlePubMedGoogle Scholar
- Wu ZG, Yu D, Li X, Xu XW. Influence of geography and environment on patterns of genetic differentiation in a widespread submerged macrophyte, Eurasian watermilfoil (Myriophyllum spicatum L., Haloragaceae). Ecol Evol. 2016;6:460-8.Google Scholar
- Qiu YX, Fu CX, Comes HP. Plant molecular phylogeography in China and adjacent regions: tracing the genetic imprints of quaternary climate and environmental change in the world’s most diverse temperate flora. Mol Phylogenet Evol. 2011;59:225–44.View ArticlePubMedGoogle Scholar
- Liu JQ, Sun YS, Ge XJ, Gao LM, Qiu YX. Phylogeographic studies of plants in China: advances in the past and directions in the future. J Syst Evol. 2012;50:267–75.View ArticleGoogle Scholar