Abstract
To assess the role of the Qinghai-Tibetan Plateau uplift in shaping the intercontinental disjunction in Northern Hemisphere, we analyzed the origin and diversification within a geological timeframe for two relict herbaceous genera, Theligonum and Kelloggia (Rubiaceae). Phylogenetic relationships within and between Theligonum and Kelloggia as well as their relatives were inferred using five chloroplast markers with parsimony, Bayesian and maximum-likelihood approaches. Migration routes and evolution of these taxa were reconstructed using Bayesian relaxed molecular clock and ancestral area reconstruction. Our results suggest the monophyly of each Theligonum and Kelloggia. Eastern Asian and North American species of Kelloggia diverged at ca.18.52 Mya and the Mediterranean species of Theligonum diverged from eastern Asian taxa at ca.13.73 Mya. Both Kelloggia and Theligonum are Tethyan flora relicts, and their ancestors might have been occurred in warm tropical to subtropical environments along the Tethys coast. The Qinghai-Tibetan Plateau separated the eastern and western Tethyan area may contribute significantly to the disjunct distributions of Theligonum, and the North Atlantic migration appears to be the most likely pathway of expansion of Kelloggia to North America. Our results highlight the importance role of the QTP uplift together with corresponding geological and climatic events in shaping biodiversity and biogeographic distribution in the Northern Hemisphere.
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Introduction
Clarifying the major factors underlying intercontinental disjunct distributions in the Northern Hemisphere has long been regarded as one of the central problems of plant biogeography1. Both the North Atlantic land bridge (NALB) and the Beringian land bridge (BLB) were available for plant migration during the Cenozoic2, but their availability for movement of particular clades of plants and animals fluctuated with changes in physical connectivity and climate2,3,4. Despite significant progresses have been achieved in understanding patterns of disjunction around the Northern Hemisphere, many important questions need to be clarified, such as the vicariance role of the Qinghai-Tibetan Plateau (QTP) uplift and subsequent effects on plant distribution in the Northern Hemisphere.
Since the Cretaceous, one of the most remarkable geological changes in Eurasia is the uplift of the QTP that resulted from the collision of the Indian Plate with Eurasian Plate in early Cenozoic5,6,7. These collision and uplift also closed the Tethys Sea followed with the permanent closure of the Turgai Seaway and contributed significantly to continentalization in Europe in the middle to late Cenozoic8. All these events opened up new corridors for biotic exchange and created various types of new habitats, which produced great effects on climate and biodiversity in the Northern Hemisphere9,10. The QTP is finally shaped as the highest and one of the most extensive plateaus in the world and one of the biodiversity hotspot in the north temperate region which harbors more than 12,000 species of vascular plants in 1500 genera11,12. Studies of plant diversification within the QTP suggested multiple mechanisms of adaptive radiation involved13. However, the impact of the QTP uplift on the biogeographic pattern in the Northern Hemisphere received relatively less attention, especially for its effects on the intercontinental disjunction in plants.
Climate cooling began in the Middle Eocene (but see Prothero, 199414 for an exception) and subsequent aridification in the Miocene–Pliocene are commonly accepted as the main causes of disjunctions between floristic elements of eastern Asia and western Eurasia from the once widespread Cenozoic flora1,2,4,15,16,17,18. The important contribution of the uplift of the QTP and downstream influences to these processes has been recognized19,20,21,22. By changing the regional climate and creating a physical barrier to flora exchange, the uplift had various impacts on the biodiversity of the QTP and adjacent areas including extinctions, floristic reorganizations and adaptive radiation23,24,25. Particularly, the QTP uplift might play an important role on shaping the well-known Madrean-Tethyan disjunction in the Northern Hemisphere.
The Madrean-Tethyan disjunction was suggested by Raven26 and Axelrod27,28 and reviewed by Liston29 and Wen and Ickert-Bond30 from phylogenetic perspectives. It was hypothesized a nearly continuous trans–Atlantic belt of Madrean-Tethyan dry and broadleaf evergreen sclerophyllous vegetation that stretched from western North America to Central Asia in the early Cenozoic at low latitudes28. The QTP is located on the east end of this belt. With continuous uplift of QTP and the spread of cool and dry climates after middle to late Eocene, broadleaved evergreen taxa were replaced by more mesic elements occupied in more restricted subhumid or dry forests across the Madrean-Tethyan regions31. The disjunct pattern is ancient and results of recent biogeographic studies mostly favor NALB migration route between the Old and the New World, but this hypothesis still needs to be verified with additional analyses30. Moreover, others have argued for the origin of this disjunct pattern via BLB or resulting from long-distance dispersal1,30,32.
Understanding of the plateau uplift history has been advanced by the application of paleontology and stable isotopes to studies of the Tibetan Plateau10. It is generally accepted that the QTP uplifted multiple times at different scales and the Himalayas reached their current elevation in the middle-late Miocene, but the uplift histories of the different terranes that comprise this plateau currently remain unclear9,10. Although the effects of QTP uplift, continentalization in Europe and aridification in Central Asia in Cenozoic in producing many biogeographic disjunctions are well recognized19,22,33,34,35,36, very few plant taxa has been evolved to elaborate the detailed date and process of biotic evolution during or after this uplift.
Theligonum L. and Kelloggia Torrey ex Bentham, two small genera from the coffee family (Rubiaceae), are excellently suited taxa to infer the role of the QTP uplift in producing disjunct distributions in the Northern Hemisphere. Both genera have a disjunct distribution along the Madrean–Tethyan belt and across the two sides of the QTP. Theligonum is a prostrate herbaceous genus occupying humid microenvironment and comprising four species: three are found at high elevations of 2500–2800 m in temperate regions of eastern Asia37,38; and one occurs at low altitude around 600–900 m in Macaronesia, the Mediterranean and the Near East39. Kelloggia includes only two species: K. chinensis Franch., that occurs in alpine meadows or forest clearances at above 3000 m on the eastern Tibetan Plateau and K. galioides Torrey that grows in open places of coniferous forests (1100–3000 m) in the western North America40,41,42,43.
Recent molecular studies identify Theligonum and Kelloggia as the closest relatives of tribe Rubieae40,44,45,46, which is centered in temperate regions and is one of the largest herbaceous tribes of Rubiaceae46,47,48. Although the sister relationship of Theligonum with Kelloggia plus Rubieae has been reported40, the biogeography and evolutionary history of the two genera have not been fully understood. Theligonum is an isolated genus of the Cenozoic evergreen forest33 and its monophyletic status has never been tested with sampling from eastern Asia. The divergence time for Kelloggia between eastern Asia and western North America was dated back to 5.42 ± 2.32 Mya based on only rbcL sequence40. According to this result, Nie et al.40 suggested the intercontinental disjunction in Kelloggia was evolved via long-distance dispersal from Asia into western North America. It did not support the Madrean-Tethyan hypothesis. However, as the authors pointed out this conclusion is based on a single gene region and limited taxa representation necessitating further analysis. Given the distribution of the eastern Asian species K. chinensis (about 3000 m, western edge of eastern Asia close to Central Asia) and the occurrence of many close relatives of Kelloggia (such as Putoria Pers. and Plocama Aiton in the tribe Paederieae and Galium) in the Mediterranean49, the genus origin and evolution seem to be closely related to the ancient Madrean-Tethyan region and the QTP uplift.
A more representative sampling of Theligonum and Kelloggia may provide higher phylogenetic resolution and improved estimation of divergence times for these taxa as well as crucial insights into the effect of the QTP uplift on plant evolution in the Northern Hemisphere. Thus, the purpose of this study was to estimate divergence times and ancestral areas for Kelloggia–Theligonum and their close relatives in order to reconstruct the biogeographical history of both Kelloggia and Theligonum. Primarily, we aimed to determine whether the current distribution of these two genera was affected by the uplift of QTP, migration along the land bridges during the late Oligocene to Miocene, long-distance dispersal, or a combination of these. As similar distribution patterns characterize other temperate plant lineages of Northern Hemisphere, such as Eremurus (Asphodelaceae), Parapteropyrum (Polygonaceae), Paliurus (Rhamnaceae) and Colutea (Fabaceae), we suppose that our findings on Kelloggia–Theligonum evolution could have broad applications. Even more generally, we hope that our analyses will encourage increased attention to the effect of the QTP uplift on plant evolution in the Northern Hemisphere.
Results
Phylogenetic analyses
The combined five–marker (rbcL, rps16, trnT–F, atpB–rbcL and psbA–trnH) data matrix consisted of 5393 nucleotides. In the combined MP analyses, 1175 characters were variable, 633 of which were potentially parsimony–informative. The MP analyses resulted in > 10,000 equally MPTs with a length of 635 steps, a consistency index of 0.83, a retention index of 0.92 and a rescaled consistency index of 0.76. For the Bayesian analysis, all partitions had a best-fit model of GTR + G, with the exception of rbcL and atpB-rbcL, for which it was TVM + I + G and TVM + I, respectively.
The topologies from the maximum parsimony, Bayesian inference and maximum likelihood analyses were congruent, but varied in the level of support for some nodes (Fig. 1). Within Kelloggia, the sister position of K. chinensis and K. galioides was well supported (BP = 93; PP = 1.00; BS = 100). Theligonum was found to be monophyletic (BP = 100; PP = 1.00; BS = 100), with a basal dichotomy into two major clades (Mediterranean, i.e. T. cynocrambe, and the eastern Asian clade), each with high support (BP = 100; PP = 1.00; BS = 100). In the eastern Asian clade, the Taiwan endemic T. formosamum was sister to the other two species. The latter species, T. macranthum from central China and T. japonicum from eastern China and Japan formed a distinct group (Fig. 1).
Divergence time analyses
The BEAST analysis generated a well–resolved tree for Theligonum and Kelloggia, the topology of which is consistent with the topologies from the MP and Bayesian analyses (Fig. 2). The uncorrelated–rates relaxed molecular clock suggested an origin of the Theligonum stem lineage in the late Eocene (35.57 million years ago (Mya); 95% HPD: 29.27–42.99 Mya; node 1 in Fig. 2). Within Theligonum, the split between the eastern Asian clade and the Mediterranean clade is dated at 13.73 Mya (95% HPD: 6.19–23.24 Mya; node 2 in Fig. 2). The age of the crown group of the eastern Asian subclade was estimated at 2.77 Mya (95% HPD: 1.03–6.01 Mya; node 4 in Tao Deng and Jian-Wen Zhang contributed equally to the work.), while the age of the crown group of the Mediterranean subclade was inferred as 3.86 Mya (95% HPD: 0.94–9.23 Mya; node 3 in Fig. 2).
The uncorrelated–rates relaxed molecular clock suggested an origin of the Kelloggia stem lineage in the early Oligocene (30.1 Mya; 95% HPD: 23.96–37.01 Mya; node 5 in Fig. 2). The spilt between the eastern Asian and the North American species was estimated at 18.52 Mya (95% HPD: 7.13–30.07 Mya; node 6 in Fig. 2).
Ancestral area reconstruction
Ancestral area reconstructions are illustrated in Fig. 3, and relative and marginal probability values of some important nodes are summarized in Table 1. Lagrange and S–DIVA analyses yielded highly similar results (differences are indicated in Table 1). Our analyses suggested western Eurasia as the ancestral area for Theligonum–Kelloggia–Rubieae clade (Fig. 3, Table 1; Mediterranean or eastern Asia in the S–DIVA analyses). Reconstruction for the Theligonum crown group indicated eastern Asia and/or western Eurasia as the most likely ancestral area. The genus splits into two lineages: one (T. cynocrambe) occurs in the western Eurasia and the other consisting of the rest of Theligonum was inferred as an ancestral area in eastern Asia. For Kelloggia, the optimizations for the stem and crown nodes indicated wide ancestral areas in eastern Asia, western North America and/or western Eurasia, and a vicariance event may have caused the disjunction between the eastern Asian and the North American clades (Fig. 3).
Discussion
Tethyan origin of Theligonum and Kelloggia
Our results provide strong molecular phylogenetic support to the monophyly of Theligonum, which is consistent with many unique morphological features that distinguish the genus in Rubiaceae38,39,50,51. In our gene tree, Theligonum is sister to a clade including Kelloggia and Rubieae with moderate support, which is in agreement with other molecular phylogenetical40,45,51 and morphological studies52. Our results also strongly support the previously reported monophyly of Kelloggia and its sister relationship with the Rubieae clade40,46. The Putorieae was found to be monophyletic and sister to the Theligonum–Kelloggia–Rubieae group, as previously reported by Backlund et al.45. Putorieae are mostly shrubs or shrublets45 while Rubieae are predominantly herbaceous species, thus the detected phylogenetic position of the exclusively herbaceous Theligonum and Kelloggia indicate their key position in the evolutionary transition from the woody to herbaceous habit in Rubiaceae.
Our dating analysis suggests that the ancestor of Theligonum has arisen in late Eocene (35.57 Mya, node 1, Fig. 2), and Kelloggia separated from Rubieae in early Oligocene (30.2 Mya, node 5, Fig. 2). Many close relatives of Theligonum and Kelloggia are distributed in western Eurasia (e.g. Plocama in the tribe Putorieae), and Rubieae also has many taxa centered in Madrean–Tethyan region (such as Galium and Rubia) and a rich endemism in the Mediterranean region and Europe40,49,53. According to our ancestral area reconstruction and dating analysis, the two genera together with Putorieae and Rubieae originated in the Eocene to Oligocene, apparently along the Tethyan coast (Fig. 3). During the Eocene to Oligocene, the Madrean–Tethyan flora represented by sclerophyllous plants adapted to subhumid climate, inhabited lower–middle latitudes forming a belt along the shores of the Tethyan region and extending even to North America54. From the start of Oligocene, once widespread evergreen and woody flora moved south in response to climatic cooling, while many deciduous and herbaceous taxa appeared18,54. Furthermore, the Tethys coast was also considered as a refugium for warm adapted species during global cooling beginning in the Middle Eocene14. The Mediterranean waters or other factors probably maintained that region as suitable and relatively stable for warm-adapted species for some time while climate cooled more drastically elsewhere in the Northern Hemisphere14. Extant species of the two studied genera living in temperate zone near the southern part of ancient Tethyan region in humid or subhumid habitats can be the relict elements of the Palaeo-Tethyan flora.
Eastern Asian – Mediterranean disjunction in Theligonum
The Mediterranean species of Theligonum diverged from the three eastern Asian relatives at about 13.73 Mya (95% HPD: 6.19–23.24 Mya) in the middle Miocene. There are two potential scenarios for this western–eastern Eurasian disjunction: (1) vicariance followed by the rapid uplift of the QTP in the Miocene55 and/or enhanced aridity in the interior of Eurasia since 14 Mya56,57, and (2) long-distance dispersal.
The first scenario has been postulated as the major factor that shaped this disjunct pattern19,58 and geological data suggest that the rapid uplift of QTP (Fig. 3) occurred about 20 Mya25,55,59,60, although the details of this process remain controversial59,61,62. This event not only dramatically changed the topography of Asia but also Asian climate. The aridification of interior Asia is believed to begin about 22–25 Mya63 mainly due to the uplift of QTP64,65,66,67 although retreat of the Paratethys Sea also contributed significantly to desertification of Central Asia68,69. Recent magneto-stratigraphic data confirmed that the QTP uplift rather than sea retreat that occurred earlier in the middle Eocene, could be linked to the aridification of Central Asia at 25–20 Mya70.
Many plant and animal taxa have been reported to evolve in a response to the early Miocene QTP uplift during 14–24 Mya, e.g. Cyananthus 71, Caragana 72, Ligularia–Cremanthodium–Parasenecio complex73 and Chinese sisorid catfish74. Divergence time for Theligonum is dated back to about 14 Mya, close to the rapid uplift of QTP in the early to mid-Miocene, although there are many debates about the uplift processes of QTP at different times and different scales10. The QTP uplifted initially in the south-central Tibet very early (around 40 Mya) then uplifted around this part since 20 Mya, especially in the eastern, southern and northern regions9. Fossils contain a large amount of paleoenvironmental information and can be used as an efficient proxy for paleoelevation10. Based on geological and fossil evidences, the majority of QTP has reached the altitude of 2,000 m at ca. 15 Mya25,62,75. The Mediterranean species T. cynocrambe occurs at lower elevation (600–900 m), while the other three species are survived at 2500–2800 m in eastern Asia. The altitudinal distribution probably suggested a hypothesis that the uplift of the QTP above ca. 3000 m in the middle Miocene together with the aridification in Central Asia formed a barrier to gene exchange between eastern Asia and the Mediterranean area. In turn, our result suggests that the QTP has likely been reached nearly 3000 m in the middle Miocene.
Other explanations (long-distance dispersal and break–up of the migration pathway north of the QTP) are unlikely. The long-distance dispersal is not supported by seed morphology and dispersal mechanism. The nut-like fruits of Theligonum contain a very thin mesocarp52,76, and therefore can be dispersed only over short distances by small mammals76,77,78. Similarly, fruits of T. cynocrambe can be distributed only over short distance by ants consuming its mucilaginous seeds39,52. Discontinued by Pliocene climate fluctuations migration through north of the QTP has been proposed as an alternative explanation for more recent Asia and Europe disjunction79. However, the divergence time (13.73 Mya) is far older than the Pliocene. In addition, Theligonum is a relict of the Tethyan flora and the basal taxon of the temperate herbaceous group (Theligonum–Kelloggia–Rubieae) within the predominantly tropical and subtropical family Rubiaceae. Therefore an area north of the QTP may have been too cold for an ancestor of Theligonum to survive.
QTP – western North American disjunction in Kelloggia
The divergence time between eastern Asian Kelloggia chinensis and western North American K. galioides is estimated to be 18.52 Mya, close to that of Theligonum. This age estimate is not fully consistent with the Madrean–Tethyan hypothesis, which predicted earlier divergence of the intercontinental disjuncts27 (Fig. 3). Fossil records are very few for herbaceous taxa in Rubiaceae and no fossils are found in Kelloggia. Only two reliable pollen fossils reported from its closely related tribe Rubieae in the Miocene80 and provided very limited insights for the biogeography of Kelloggia. However, both paleontological and geological evidences suggested that the NALB which connected North America and Europe via southern Greenland and Scotland, and probably some island chains, served as the migration route for tropical, subtropical and temperate elements from the early to middle Cenozoic2,4,81. Nie et al.40 rejected the NALB pathway because the divergence time of Kelloggia in their analysis was too recent (5.42 ± 2.32 Mya). The present dating analysis based on a larger number of gene regions and credible fossil records, update the divergence time to be 18.52 Mya (95% HDP: 7.13–30.07 Mya), which is within the believed upper limit of 15 Mya18,82,83. Many thermophilic plants and a few animals are believed to have crossed the Atlantic within the past 15 Mya, including Bromeliaceae, Melastomataceae and Rapateaceae84,85. The BLB served another possible Cenozoic land connection between Eurasia and North America that contributed mainly to intercontinental temperate taxa exchange until about 3.5 Mya2,3,4,86,87.
According to our estimated divergence time, both the BLB and NALB could have acted as possible migration pathways for Kelloggia. Although, another hypothesis of long-distance dispersal (LDD) via birds is potentially possible in Kelloggia because its fruits possess hooked bristles. A similar situation is found in another disjunct genus Osmorhiza with hooked appendages on fruits88. The modern limited geographic range in each continent may be due to the limited availability of habitats in western North America and in the Hengduan Mountains. If we accept that Kelloggia originated within tropical Rubiaceae in the Tethyan region, and considering the fact that many close genera relatives occur in the extant Mediterranean region, the NALB hypothesis appears to be the most likely migration route. Kelloggia, as one of the Tethyan elements, might have expanded to North America via the NALB in the Oligocene to early Miocene (Fig. 3). Similar to Theligonum, the rapid uplift of QTP and aridification of Central Asia in early Miocene might cause its disjunction, and the climate cooling could be responsible for its modern restricted distribution.
Although the genus Kelloggia appears to have originated in the late Eocene to early Oligocene, modern species of Kelloggia, like Theligonum, arose much later (in Pliocene). Given the highest extinction frequency of Cenozoic relict taxa in Europe4,16,18, extinction of Kelloggia in Europe might occur during the climate change, and that could explain the results in our ancestor area reconstruction. The long branches between stem and crown of clades from each continent (clades 5 and 6 in Fig. 2) also suggest that extinction might be common in both genera.
Conclusion
Our dating analysis and ancestral area reconstructions results suggest that both Kelloggia and Theligonum are Tethyan flora relicts, and the distribution area of their ancestors might have been warm tropical to subtropical environments along the Tethys coast in Eurasia. NALB appears to be the most likely pathway of expansion of Kelloggia to North America, though the LDD cannot be ruled out. A similar divergence time in Kelloggia and Theligonum (18.52 and 13.73 Mya) might reflect common historical events in their evolutionary history. The uplift of QTP in the early Miocene and aridification in Central Asia probably triggered separation of eastern and western parts of the ranges in both Kelloggia and Theligonum. Climate cooling since mid-Miocene in Northern Hemisphere caused range shifts in these two taxa to the modern distribution area, where Theligonum survived in moist micro-habitats of southwestern Eurasia while Kelloggia got extinct like many other Cenozoic relict taxa in this region18.
Methods
Taxon sampling
All species from both Theligonum and Kelloggia were included in this study. We newly sequenced three eastern Asian species of Theligonum (11 accessions), one species (T. cynocrambe) from Turkey (1 accession), and the Kelloggia species (5 accessions). Voucher information and accession numbers of newly sequenced taxa are provided in the Appendix S1. We also included 3 accessions of Theligonum and 5 accessions of Kelloggia from GenBank to cover the whole geographic range of both disjunct regions (Appendix S2). Close relatives of Theligonum and Kelloggia such as Rubieae, Putorieae, and Paederieae45,51,89, and the more distantly related Gelsemium 90,91 were included as outgroups in our phylogenetic analyses (Appendix S2).
DNA extraction, amplification, and sequencing
Total genomic DNA was isolated from silica gel–dried leaf material using a Universal Genomic DNA Extraction Kit (Takara, Dalian, China). Five chloroplasts (the rbcL gene; the rps16 intron; the trnT–F region; the atpB–rbcL and psbA–trnH intergenic spacers) were selected for phylogenetic inference. For trnT–F regions, primers A (or A1) and D, as well as c and f as in Taberlet et al.92 and Bremer et al.93 were used with the internal. For rbcL, primers Z1 and 3′995 were used. The atpB-rbcL and psbA-trnH spacers were amplified and sequenced using the primers as described by Manen et al.96 and Sang et al.97, respectively. The rps16 intron was amplified and sequenced with primers F and 2 R98,99. All polymerase chain reactions (PCRs) were run in a PTC–100 thermocycler (MJ Research, Ramsey, MN, USA). PCR products were purified using an agarose gel DNA purification kit (Takara, Shiga, Japan), following the manufacturer’s instructions. Sequencing was performed with BigDye Terminator 3.1 (Applied Biosystems, Foster City, CA, USA) on an ABI PRISM 3730 Sequencer using the same primers as employed for the PCR amplifications. All sequences were analyzed and assembled with Sequencher ver.4.14 (Gene Code, Ann Arbor, MI, USA).
Sequence Alignment and Phylogenetic Analyses
DNA Baser v.3 (http://www.DnaBaser.com) was used to evaluate the chromatograms for base confirmation and to edit contiguous sequences. Multiple–sequence alignment was performed by MAFFT v.6100, using the default alignment parameters followed by manual adjustment in Se–Al v2.0a11 (http://tree.bio.ed.ac.uk/software/seal/), and gaps were treated as missing data.
DNA molecular phylogenies were reconstructed using maximum parsimony (MP), Bayesian inference (BI) and Maximum likelihood (ML). The parsimony analyses were conducted under the option heuristic search with 10 random stepwise additions and tree–bisection–reconnection (TBR) branch swapping with PAUP* version 4.0 b10101. Zero–length branches were collapsed and gaps were treated as missing data. Subsequently, parsimony bootstrap (BP) analyses102 with 1000 replicates were performed under the option fast and stepwise addition to evaluate the robustness of the MP trees.
Maximum likelihood (ML) analyses were run in RAxMLGUI 1.3103, followed by 1000 replicates of thorough Bootstrap (BS). Bayesian inference of likelihood was implemented by using with MrBayes version 3.1.2104. The best-fit models with parameters of nucleotide substitution for the individual data partitions were determined with jModeltest 2.1.3105 using the Akaike Information Criterion. For BI analyses, we ran two independent analyses consisting of four Markov chains sampled every 1000 generations for 10 million generations. After discarding the first 2 million generations as burn–in, the remaining trees from both analyses were pooled for a consensus tree. The proportions of bifurcations found in this consensus tree are given as Bayesian posterior probabilities (PP).
Divergence Time Estimates and Fossil Calibration
Estimation of divergence times was performed in a Bayesian framework with BEAST version 1.7.5106 using the XSEDE package available online through the CIPRES Science Gateway 3.3107. After assessing the sequences generated and those available from GenBank, we chose to use the combined rbcL, rps16, trnT-F, and atpB-rbcL data to estimate the divergence time of Theligonum and Kelloggia. PsbA-trnH was not used due to its high sequences variation on the family level. With our focus on the divergence time of Theligonum and Kelloggia, and with the consideration of minimizing the influence from topological uncertainties in our analyses on dating of the phylogeny, we excluded some Theligonum and Kelloggia taxa. To allow multiple fossil calibrations in a broader phylogenetic framework of Rubiaceae, sequences of 68 additional taxa were obtained from GenBank (see Appendix S2). Furthermore, Gelsemium sempervirens (L.) J.St.-Hil. From Gelsemiaceae was selected as the remote outgroup in our dating analysis.
The input files were created using BEAUti 1.7.5, in which three partitions were specified. The best performing evolutionary model for each molecular marker was identified using jModelTest 2.1.1105. For the distribution of divergence times, a pure birth branching process (Yule model) was chosen as a prior. We ran two independent Markov chains, each for 100,000,000 generations, initiated with a random starting tree, and sampled every 10,000 generations. From collected samples, 15% were eliminated (treated as burn–in). All log and tree files from independent runs were combined using LogCombiner 1.7.5106. The results were summarized using the maximum clade credibility (MCC) tree option in TreeAnnotator 1.7.5106. Tracer 1.5 was used to check for convergence between the runs106. The tree was visualized using FigTree 1.4108 and the means and 95% higher posterior densities (HPD) could be obtained from it. The 95% HPD represents the shortest interval that contains 95% of the sampled values from the posterior106.
Four fossils from Rubiaceae (two fruits and two pollens) were selected as calibration points in our analyses, which have been widely used to estimate divergence times in various groups in the family40,90,91,109,110,111. The fruit fossil of Cephalanthus from the late Eocene to the Pliocene (see more in Antonelli et al.90), considered as the most convincing Rubiaceae fossils. The oldest fossil of Cephalanthus was found from Kireevski in western Siberia in the late Eocene112,113 and is used here to place a normal constraint of the stem age of Cephalanthus as 33.9 ± 1.0 Mya. Another well–preserved fruit fossil of a head–shaped infructescence was described as a new species, Morinda chinensis Shi, Liu & Jin, from the Changchang Formation in Hainan of China114. Because Morinda is paraphyletic in tribe Morideae115 and the phylogenetic position of this fossil species is unclear, we took a conservative approach and used this fossil to calibrate the crown age of the tribe with the prior set to 44.5 ± 3.0 Mya, which falls into the fossil age estimated from the late early Eocene to the early late Eocene114.
Most of the reported Rubiaceae fossils are dispersed pollen grains of a common tricolporate type. However, we used only the two most reliable pollen fossils in our analyses. The oldest pollen fossils of Faramea from the late Eocene (34–40 Mya) in Panama to the Pliocene in Veracruz, Mexico80, which are characterized by the orientation of the bacula at the apertures (two– to four–porate) and the size and the shape of the pollen91,116. Thus, the Faramea stem node was constrained at 37 ± 1.0 Mya. Two pollen fossils of Scyphiphora were reported at 16 Mya from Japan and at 23 Mya from the Marshall Islands in the northern Pacific Ocean117,118. Scyphiphora is the only extant genus of Rubiaceae that inhabits mangrove vegetation, and its pollen character is unique in the family, with distinct pores having a protruding papilla–like rim91. We therefore used 23 ± 1.0 Mya as a normal prior for the Scyphiphora node.
For rooting the tree, we followed Antonelli et al.90 to set the stem Rubiaceae age as 78 ± 1.0 Mya based on the crown age estimate of Gentianales119.
Biogeographic analyses
Four biogeographical areas of endemism were delimited according to the main geographic distribution of Theligonum, Kelloggia, and its close relatives (Fig. 3): A = eastern Asia; B = the Mediterranean (including western Asia and north Africa); C = North America; D = Africa, but excluding north Africa.
Parsimony–based statistical dispersal–vicariance analysis (S–DIVA), accounting for uncertainty of both phylogenetic and ancestral area reconstructions120,121,122,123 was performed by RASP 2.0b120,121, and likelihood–based analyses under the dispersal–extinction–cladogenesis (DEC) model was performed with Lagrange 2.0.1124,125 to reconstruct ancestral areas at internal nodes. We conducted analyses with maximum alternative scenarios at each node set to 3 and 2 to examine the effect of constraints on reconstructed ancestral distributions126.
For the S–DIVA analyses, 8000 input trees were selected by resampling from the post–burn–in sample of the BEAST analysis at lower frequency using Log Combiner. Relative frequencies of ancestral areas reconstructed for each node were recorded and plotted onto the MCC tree from the BEAST analysis. The Lagrange online configurator (http://www.reelab.net/lagrange/configurator/index) was used to create input files. The MCC tree from the BEAST analysis was used as input trees.
References
Raven, P. H. Plant species disjunctions: a summary. Ann. Mo. Bot. Gard. 59, 234–246 (1972).
Tiffney, B. H. The Eocene North Atlantic land bridge: its importance in tertiary and modern phytogeography of the Northern hemisphere. J. Arnold Arboretum 66, 243–273 (1985).
Tiffney, B. H. & Manchester, S. R. The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the Northern Hemisphere tertiary. Int. J. Plant Sci. 162, S3–S17 (2001).
Wen, J. Evolution of eastern Asian and eastern North American disjunct distributions in flowering plants. Annu. Rev. Ecol. Syst. 30, 421–455 (1999).
Coleman, M. & Hodges, K. Evidence for Tibetan Plateau Uplift before 14-Myr Ago from a New Minimum Age for East-West Extension. Nature 374, 49–52 (1995).
Rowley, D. B. & Currie, B. S. Palaeo-altimetry of the late Eocene to Miocene Lunpola basin, central Tibet. Nature 439, 677–681, https://doi.org/10.1038/Nature04506 (2006).
Royden, L. H., Burchfiel, B. C. & van der Hilst, R. D. The geological evolution of the Tibetan plateau. Science 321, 1054–1058, https://doi.org/10.1126/Science.1155371 (2008).
Rögl, F. Mediterranean and Paratethys. Facts and hypotheses of an Oligocene to Miocene paleogeography (short overview). Geol. Carpath. 50, 339–349 (1999).
Mulch, A. & Chamberlain, C. P. Earth science: the rise and growth of Tibet. Nature 439, 670–671, https://doi.org/10.1038/439670a (2006).
Liu, X. H., Xu, Q. & Ding, L. Differential surface uplift: Cenozoic paleoelevation history of the Tibetan Plateau. Sci. China E. 59, 2105–2020, https://doi.org/10.1007/s11430-015-5486-y (2016).
Wu, Z. Y. Hengduan mountain flora and her significance. J. Jpn Bot. 63, 297–311 (1988).
Li, X. W. & Li, J. A preliminary floristic study on the seed plants from the region of Hengduan Mountain. Acta Bot. Yunnan. 15, 217–231 (1993).
Wen, J., Zhang, J. Q., Nie, Z. L., Zhong, Y. & Sun, H. Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau. Front. Gen. 5, 4, https://doi.org/10.3389/fgene.2014.00004 (2014).
Prothero, D. R. The Eocene-Oligocene transition: Paradise lost. (Columbia University Press, 1994).
Wolfe, J. A. Some aspects of plant geography of the Northern Hemisphere during the late Cretaceous and Tertiary. Ann. Mo. Bot. Gard. 62, 264–279 (1975).
Tiffney, B. H. Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. J. Arnold Arboretum 66, 73–94 (1985).
Milne, R. I. Northern hemisphere plant disjunctions: a window on tertiary land bridges and climate change? Ann. Bot. 98, 465–472 (2006).
Milne, R. I. & Abbott, R. J. The origin and evolution of Tertiary relict floras. Adv. Bot. Res. 38, 281–314 (2002).
Sun, H. Tethys retreat and Himalayas-Hengduanshan Mountains uplift and their significance on the origin and development of the Sino-Himalayan elements and alpine flora. Acta Bot. Yunnan. 24, 273–228 (2002).
Sun, H., McLewin, W. & Fay, M. F. Molecular phylogeny of Helleborus (Ranunculaceae), with an emphasis on the East Asian-Mediterranean disjunction. Taxon, 1001–1018 (2001).
Sun, H. & Li, Z. Qinghai-Tibet Plateau uplift and its impact on Tethys flora. Adv. Earth Sci. 18, 852–862 (2003).
Chen, Y.-S. et al. Out-of-India dispersal of Paliurus (Rhamnaceae) indicated by combined molecular phylogenetic and fossil evidence. Taxon 66, 78–90, https://doi.org/10.12705/661.4 (2017).
Ni, J. A simulation of biomes on the Tibetan Plateau and their responses to global climate change. Mt. Res. Dev. 20, 80–89 (2000).
Che, J. et al. Spiny frogs (Paini) illuminate the history of the Himalayan region and Southeast Asia. Proc. Natl. Acad. Sci. USA. 107, 13765–13770 (2010).
Shi, Y., Li, J. & Li, B. Uplift of the Qinghai-Xizang(Tibetan) Plateau and East Asia environmental change during late Cenozoic. Acta Geogr. Sin. 54, 10–21 (1999).
Raven, P. H. In Plant Life of South-West Asia (eds P. Davis, P. Harper, & I. Hedge) 119–134 (The Botanical Society of Edinburgh, The University Press, 1971).
Axelrod, D. I. In Mediterranean Type Ecosystems - Origin and Structure (eds F. di Castri & H.A. Mooney) 225–277 (Springer Verlag, 1973).
Axelrod, D. I. Evolution and Biogeography of Madrean-Tethyan Sclerophyll Vegetation. Ann. Mo. Bot. Gard. 62, 280–334 (1975).
Liston, A. Biogeographic relationships between the Mediterranean and North American floras: insights from molecular data. Lagascalia 19, 323–330 (1997).
Wen, J. & Ickert-Bond, S. M. Evolution of the Madrean-Tethyan disjunctions and the North and South American amphitropical disjunctions in plants. J. Syst. Evol. 47, 331–348, https://doi.org/10.1111/j.1759-6831.2009.00054.x (2009).
Xie, L., Yang, Z.-Y., Wen, J., Li, D.-Z. & Yi, T.-S. Biogeographic history of Pistacia (Anacardiaceae), emphasizing the evolution of the Madrean-Tethyan and the eastern Asian-Tethyan disjunctions. Mol. Phylogenet. Evol. 77, 136–146 (2014).
Raven, P. H. & Axelrod, D. I. History of the flora and fauna of Latin America. Am. Sci. 63, 420–429 (1975).
Tang, Y. C. On the Affinities and the Role of the Chinese Flora. Act. Bot. Yunnan. 22, 1–26 (2000).
Axelrod, D. I., Al-Shehbaz, I. & Raven, R. H. In Floristic Characteristics and Diversity of East Asian Plants (eds A. L. Zhang & S. G. Wu) 43-55 (China Higher Education Press, 1998).
Zhang, Z. Y., Fan, L. M., Yang, J. B., Hao, X. J. & Gu, Z. J. Alkaloid polymorphism and ITS sequence variation in the Spiraea japonica complex (Rosaceae) in China: traces of the biological effects of the Himalaya-Tibet plateau uplift. Am. J. Bot. 93, 762–769 (2006).
Tu, T. Y., Volis, S., Dillon, M. O., Sun, H. & Wen, J. Dispersals of Hyoscyameae and Mandragoreae (Solanaceae) from the New World to Eurasia in the early Miocene and their biogeographic diversification within Eurasia. Mol. Phylogenet. Evol. 57, 1226–1237, https://doi.org/10.1016/J.Ympev.2010.09.007 (2010).
Yamazaki, T. In Flora of Japan, IIIa (eds K. Iwatsuki, T. Yamazaki, D. E. Boufford, & H. Ohba) 241 (Kodänsha, 1993).
Chen, T. et al. In Flora of China,Vol. 19 (eds C. Y. Wu & R. Peter) (Science and Press & Missouri Botanical Garden Press, 2011).
Ulbrich, E. Über die Gattung Thelygonum SAuv. ex L. 1753. Notizblatt des Königl. botanischen Gartens und Museums zu Berlin 11, 889–902 (1933).
Nie, Z.-L., Wen, J., Sun, H. & Bartholomew, B. Monophyly of Kelloggia Torrey ex Benth. (Rubiaceae) and evolution of its intercontinental disjunction between western North America and eastern Asia. Am. J. Bot. 92, 642–652, https://doi.org/10.3732/ajb.92.4.642 (2005).
Bentham, G. & Hooker, J. Genera plantarum, vol. 3. (L. Reeve, 1883).
Cronquist, A., Ownbey, M. & Thompson, J. Vascular plants of the Pacific Northwest. (University of Washington Press, 1971).
Hickman, J. C. The Jepson manual: higher plants of California. (University of California Press 1993).
Robbrecht, E. & Manen, J. F. The major evolutionary lineages of the coffee family (Rubiaceae, angiosperms). Combined analysis (nDNA and cpDNA) to infer the position of Coptosapelta and Luculia, and supertree construction based on rbcL, rps16, trnL-trnF and atpB-rbcL data. A new classification in two subfamilies, Cinchonoideae and Rubioideae. Syst. Geogr. Pl. 76, 85–146 (2006).
Backlund, M., Bremer, B. & Thulin, M. Paraphyly of Paederieae, recognition of Putorieae and expansion of Plocama (Rubiaceae-Rubioideae). Taxon 56, 315–328 (2007).
Soza, V. L. & Olmstead, R. G. Molecular systematics of tribe Rubieae (Rubiaceae): Evolution of major clades, development of leaf-like whorls, and biogeography. Taxon 59, 755–771 (2010).
Robbrecht, E. Tropical woody Rubiaceae. Opera Botanica Belgica 1, 599–602 (1988).
Manen, J. F. & Natali, A. Comparison of the evolution of ribulose-1, 5-biphosphate carboxylase (rbcL) and atpB-rbcL noncoding spacer sequences in a recent plant group, the tribe Rubieae (Rubiaceae). J. Mol. Evol. 41, 920–927 (1995).
Puff, C. The Delimitation of the Tribe Anthospermeae and Its Affinities to the Paederieae (Rubiaceae). Bot. J. Linnean Soc. 84, 355–377 (1982).
Praglowski, J. The pollen morphology of the Theligonaceae with reference to taxonomy. Pollen Spores 15, 385–396 (1973).
Bremer, B. & Manen, J. F. Phylogeny and classification of the subfamily Rubioideae (Rubiaceae). Plant Syst. Evol. 225, 43–72 (2000).
Rutishauser, R., Decraene, L. P. R., Smets, E. & Mendoza-Heuer, I. Theligonum cynocrambe: Developmental morphology of a peculiar rubiaceous herb. Plant Syst. Evol. 210, 1–24 (1998).
Mabberley, D. J. The plant-book: a portable dictionary of the vascular plants. (1997).
Axelrod, D. I. Evolution and biogeography of Madrean-Tethyan sclerophyll vegetation. Ann. Mo. Bot. Gard. 62, 280–334 (1975).
Harrison, T. M., Copeland, P., Kidd, W. & Yin, A. Raising tibet. Science 255, 1663–1670 (1992).
An, Z. S. et al. Changes of the monsoon-arid environment in China and growth of the Tibetan Plateau since the Miocene. Quaternary Sci. 26, 678–693 (2006).
Fortelius, M. et al. Late Miocene and Pliocene large land mammals and climatic changes in Eurasia. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, 219–227 (2006).
Zhang, Z., Fan, L., Yang, J., Hao, X. & Gu, Z. Alkaloid polymorphism and ITS sequence variation in the Spiraea japonica complex (Rosaceae) in China: traces of the biological effects of the Himalaya-Tibet Plateau uplift. Am. J. Bot. 93, 762–769 (2006).
Copeland, P. et al. Thermal evolution of the Gangdese batholith, southern Tibet: A history of episodic unroofing. Tectonics 14, 223–236 (1995).
Molnar, P., England, P. & Martinod, J. Mantle Dynamics, Uplift of the Tibetan Plateau, and the Indian Monsoon. Rev. Geophys. 31, 357–396 (1993).
Spicer, R. A. et al. Constant elevation of southern Tibet over the past 15 million years. Nature 421, 622–624 (2003).
Shi, Y. & MCTang, M.,Y. The relation of second rising in Qinghai-Xizang Plateau and Asia Monsoon. Sci. China D. 28, 263–271 (1998).
Guo, Z. et al. Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China. Nature 416, 159–163 (2002).
Fang, X. et al. High-resolution magnetostratigraphy of the Neogene Huaitoutala section in the eastern Qaidam Basin on the NE Tibetan Plateau, Qinghai Province, China and its implication on tectonic uplift of the NE Tibetan Plateau. Earth Planet. Sci. Lett. 258, 293–306 (2007).
Sun, J., Li, Y., Zhang, Z. & Fu, B. Magnetostratigraphic data on Neogene growth folding in the foreland basin of the southern Tianshan Mountains. Geology 37, 1051–1054 (2009).
Kutzbach, J., Guetter, P., Ruddiman, W. & Prell, W. Sensitivity of climate to late Cenozoic uplift in Southern Asia and the American West: Numerical experiments. J. Geophys. Res. 94(18393–18318), 18407 (1989).
Liu, X., Kutzbach, J. E., Liu, Z., An, Z. & Li, L. The Tibetan Plateau as amplifier of orbital-scale variability of the East Asian monsoon. Geophys. Res. Lett. 30, 1839 (2003).
Zhang, Z. S., Wang, H., Guo, Z. & Jiang, D. What triggers the transition of palaeoenvironmental patterns in China, the Tibetan Plateau uplift or the Paratethys Sea retreat? Palaeogeogr. Palaeoclimatol. Palaeoecol. 245, 317–331 (2007).
Ramstein, G., Fluteau, F., Besse, J. & Joussaume, S. Effect of orogeny, plate motion and land-sea distribution on Eurasian climate change over the past 30 million years. Nature 386, 788–795 (1997).
Xiao, G. et al. Evidence for northeastern Tibetan Plateau uplift between 25 and 20Ma in the sedimentary archive of the Xining Basin, Northwestern China. Earth Planet. Sci. Lett. 317, 185–195 (2012).
Zhou, Z. et al. Phylogenetic and biogeographic analyses of the Sino-Himalayan endemic genus Cyananthus (Campanulaceae) and implications for the evolution of its sexual system. Mol. Phylogenet. Evol. 68, 482–497, https://doi.org/10.1016/j.ympev.2013.04.027 (2013).
Zhang, M. L. & Fritsch, P. W. Evolutionary response of Caragana (Fabaceae) to Qinghai–Tibetan Plateau uplift and Asian interior aridification. Plant Syst. Evol. 288, 191–199 (2010).
Liu, J. Q., Wang, Y. J., Wang, A. L., Hideaki, O. & Abbott, R. J. Radiation and diversification within the Ligularia– Cremanthodium– Parasenecio complex (Asteraceae) triggered by uplift of the Qinghai-Tibetan Plateau. Mol. Phylogenet. Evol. 38, 31–49 (2006).
Guo, X., He, S. & Zhang, Y. Phylogeny and biogeography of Chinese sisorid catfishes re-examined using mitochondrial cytochrome b and 16S rRNA gene sequences. Mol. Phylogenet. Evol. 35, 344–362 (2005).
Li, J. & Fang, X. Research on the uplift of the Qinghai-Xizang Plateau and environmental changes. Chin. Sci. Bull. 43, 1569–1574 (1998).
Eriksson, O. & Bremer, B. Pollination Systems, Dispersal Modes, Life Forms, and Diversification Rates in Angiosperm Families. Evolution 46, 258–266, https://doi.org/10.2307/2409820 (1992).
Eriksson, O. & Bremer, B. Fruit characteristics, life forms, and species richness in the plant family Rubiaceae. Am. Nat. 138, 751–761 (1991).
Bremer, B. & Eriksson, O. Evolution of fruit characters and dispersal modes in the tropical family Rubiaceae. Biol. J. Linn. Soc. 47, 79–95, https://doi.org/10.1111/j.1095-8312.1992.tb00657.x (1992).
Carlson, S. E., Linder, H. P. & Donoghue, M. J. The historical biogeography of Scabiosa (Dipsacaceae): implications for Old World plant disjunctions. J. Biogeogr. 39, 1086–1100 (2012).
Graham, A. Fossil Record of the Rubiaceae. Annals of the Missouri Botanical Garden 96, 90–108, https://doi.org/10.3417/2006165 (2009).
Tiffney, B. H. Geographic and climatic influences on the Cretaceous and Tertiary history of Euramerican floristic similarity. Acta Universitatis Carolinae - Geologica 44, 5–16 (2000).
Schnitker, D. North Atlantic oceanography as a possible cause of Antarctic glaciation and eutrophication. Nature 284, 615–616 (1980).
Poole, D. A. R. & Vorren, T. O. Miocene to Quaternary paleoenvironments and uplift history of the mid Norwegian shelf. Mar. Geol. 115, 173–205 (1993).
Renner, S. Plant dispersal across the tropical Atlantic by wind and sea currents. Int. J. Plant Sci. 165, S23–S33 (2004).
De Queiroz, A. The resurrection of oceanic dispersal in historical biogeography. Trends Ecol. Evol. 20, 68–73 (2005).
Gladenkov, A. Y., Oleinik, A. E., Marincovich, L. & Barinov, K. B. A refined age for the earliest opening of Bering Strait. Palaeogeogr. Palaeoclimatol. Palaeoecol. 183, 321–328, https://doi.org/10.1016/S0031-0182(02)00249-3 (2002).
Wen, J., Nie, Z.-L. & Ickert-Bond, S. M. Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to Neogene. J. Syst. Evol. 54, 469–490, https://doi.org/10.1111/jse.12222 (2016).
Yi, T.-s, Jin, G.-h & Wen, J. Chloroplast capture and intra- and inter-continental biogeographic diversification in the Asian – New World disjunct plant genus Osmorhiza (Apiaceae). Mol. Phylogenet. Evol. 85, 10–21, https://doi.org/10.1016/j.ympev.2014.09.028 (2015).
Rydin, C., Razafimandimbison, S. G., Khodabandeh, A. & Bremer, B. Evolutionary relationships in the Spermacoceae alliance (Rubiaceae) using information from six molecular loci: insights into systematic affinities of Neohymenopogon and Mouretia. Taxon 58, 793–810 (2009).
Antonelli, A., Nylander, J. A. A., Persson, C. & Sanmartin, I. Tracing the impact of the Andean uplift on Neotropical plant evolution. Proc. Natl. Acad. Sci. U. S. A. 106, 9749–9754, https://doi.org/10.1073/Pnas.0811421106 (2009).
Bremer, B. & Eriksson, T. Time tree of Rubiaceae: phylogeny and dating the family, subfamilies, and tribes. Int. J. Plant Sci. 170, 766–793, https://doi.org/10.1086/599077 (2009).
Taberlet, P., Gielly, L., Pautou, G. & Bouvet, J. Universal Primers for Amplification of 3 Noncoding Regions of Chloroplast DNA. Plant Mol. Biol. 17, 1105–1109 (1991).
Bremer, B. et al. Phylogenetics of asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higher taxonomic levels. Mol. Phylogenet. Evol. 24, 274–301 (2002).
Zurawski, G., Perrot, B., Bottomley, W. & Paul, R. W. The structure of the gene for the large subunit of ribulose 1,5-bispho- sphate carboxylase from spinach chloroplastDNA. Molec. Biol. 9, 3251–3270 (1981).
Olmstead, R. G., Bremer, B., Scott, K. M. & Palmer, J. D. A parsimony analysis of the Asteridae sensu lato based on rbcL sequences. Ann. Mo. Bot. Gard. 80, 700–722 (1993).
Manen, J.-F., Natali, A. & Ehrendorfer, F. Phylogeny of Rubiaceae-Rubieae inferred from the sequence of a cpDNA intergene region. Plant Syst. Evol. 190, 195–211 (1994).
Sang, T., Crawford, D. J. & Stuessy, T. F. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). Am. J. Bot. 84, 1120–1136 (1997).
Oxelman, B., Liden, M. & Berglund, D. Chloroplast rps16 intron phylogeny of the tribe Sileneae (Caryophyllaceae). Plant Systematics and Evolution 206, 393–410 (1997).
Andersson, L. & Rova, J. H. The rps16 intron and the phylogeny of the Rubioideae (Rubiaceae). Plant Syst. Evol. 214, 161–186 (1999).
Katoh, K. & Toh, H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9, 286–298, https://doi.org/10.1093/bib/bbn013 (2008).
Swofford, D. L. PAUP*: Phylogenetic analysis using parsimony (*and other methods), version 4.0b10. (Sinauer Associates, 2003).
Felsenstein, J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791 (1985).
Silvestro, D. & Michalak, I. raxmlGUI: a graphical front-end for RAxML. Org. Divers. Evol. 12, 335–337, https://doi.org/10.1007/s13127-011-0056-0 (2012).
Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001).
Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772–772 (2012).
Drummond, A. J. & Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214; doi:Artn 214 (2007).
Miller, M. A., Pfeiffer, W. & Schwartz, T. In Gateway Computing Environments Workshop (GCE), 2010. 1– (IEEE).
Rambaut, A. FigTree v.1.4. Available at: http://tree.bio.ed.ac.uk/software/figtree/ (last accessed 11 March 2013) (2009).
Smedmark, J. E. E., Eriksson, T. & Bremer, B. Divergence time uncertainty and historical biogeography reconstruction - an example from Urophylleae (Rubiaceae). J. Biogeogr. 37, 2260–2274, https://doi.org/10.1111/j.1365-2699.2010.02366.x (2010).
Huang, W.-P. et al. Molecular phylogenetics and biogeography of the eastern Asian–eastern North American disjunct Mitchella and its close relative Damnacanthus (Rubiaceae, Mitchelleae). Bot. J. Linnean Soc. 171, 395–412, https://doi.org/10.1111/j.1095-8339.2012.01321.x (2013).
Nie, Z.-L., Deng, T., Meng, Y., Sun, H. & Wen, J. Post-Boreotropical dispersals explain the pantropical disjunction in Paederia (Rubiaceae). Ann. Bot. 111, 873–886, https://doi.org/10.1093/aob/mct053 (2013).
Dorofeev, P. I. Tertiary floras of western Siberia. (Izd-vo Akademii nauk SSSR, 1963).
Dorofeev, P. I. New data about Tertiary floras of Kirrenskiy ravine on the Ob River. Doklady Akademii Nauk SSSR 133, 211–213 (1960).
Shi, X., Jin, J., Ye, C. & Liu, W. First fruit fossil record of Morinda (Rubiaceae) from China. Rev. Palaeobot. Palynology 179, 13–16 (2012).
Razafimandimbison, S. G., McDowell, T. D., Halford, D. A. & Bremer, B. Molecular phylogenetics and generic assessment in the tribe Morindeae (Rubiaceae-Rubioideae): How to circumscribe Morinda L. to be monophyletic? Mol. Phylogenet. Evol. 52, 879–886 (2009).
Erdtman, G. Pollen morphology and plant taxonomy. (Hafner, 1966).
Leopold, E. Miocene pollen and spore flora of Eniwetok Atoll, Marshall Island. Geol. Surv. Prof. Paper 260-II, 1133–1185 (1969).
Saenger, P. Mangrove vegetation: an evolutionary perspective. Mar. Freshwater Res. 49, 277–286 (1998).
Bremer, K., Friis, E. M. & Bremer, B. Molecular phylogenetic dating of asterid flowering plants shows early Cretaceous diversification. Syst. Biol. 53, 496–505 (2004).
Yu, Y., Harris, A. J. & He, X. J. RASP (Reconstruct Ancestral State in Phylogenies) 2.1beta. Available athttp://mnh.scu.edu.cn/soft/blog/RASP (2013).
Yu, Y., Harris, A. J. & He, X. J. S-DIVA (Statistical Dispersal-Vicariance Analysis): A tool for inferring biogeographic histories. Mol. Phylogenet. Evol. 56, 848–850 (2010).
Harris, A. J. & Xiang, Q. Y. Estimating ancestral distributions of lineages with uncertain sister groups: a statistical approach to Dispersal–Vicariance Analysis and a case using Aesculus L.(Sapindaceae) including fossils. J. Syst. Evol. 47, 349–368 (2009).
Nylander, J. A. A., Olsson, U., Alstrom, P. & Sanmartin, I. Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal-vicariance analysis of the thrushes (Aves: Turdus). Syst. Biol. 57, 257–268 (2008).
Ree, R. H. & Smith, S. A. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst. Biol. 57, 4–14 (2008).
Ree, R. H., Moore, B. R., Webb, C. O. & Donoghue, M. J. A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution 59, 2299–2311 (2005).
Kodandaramaiah, U. Use of dispersal–vicariance analysis in biogeography–a critique. J. Biogeogr. 37, 3–11 (2010).
Acknowledgements
This study was supported by grants from the Major Program of National Natural Science Foundation of China (31590823), National Natural Science Foundation of China (31370244, 31570211, 31700165) and the West Light Foundation of the Chinese Academy of Sciences. We are grateful to Dr. Doug Soltis, Dr. Carina Hoorn and Dr. Wei-Ping Huang for valuable comments on the early version of the manuscript.
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Z.L.N., H.S., and T.D. conceived the idea, collected the data and conducted the analysis. All authors contributed to the writing.
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Deng, T., Zhang, JW., Meng, Y. et al. Role of the Qinghai-Tibetan Plateau uplift in the Northern Hemisphere disjunction: evidence from two herbaceous genera of Rubiaceae. Sci Rep 7, 13411 (2017). https://doi.org/10.1038/s41598-017-13543-5
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DOI: https://doi.org/10.1038/s41598-017-13543-5
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