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Systematics and Phytogeography |
2Department of Biological Science, School of Science, Osaka Prefecture University, Sakai, Osaka 599-8531, Japan 3Department of Botany, National Museum of Natural History, MRC166, Smithsonian Institution, Washington, D.C. 20013-7012 USA; and Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxinchun 20, Xiangshan, Beijing 100093, P. R. China
Received for publication June 22, 2005. Accepted for publication October 25, 2005.
ABSTRACT
Seventy-nine species representing 12 genera of Vitaceae were sequenced for the trnL-F spacer, 37 of which were subsequently sequenced for the atpB-rbcL spacer and the rps16 intron. Phylogenetic analysis of the combined data provided a fairly robust phylogeny for Vitaceae. Cayratia, Tetrastigma, and Cyphostemma form a clade. Cyphostemma and Tetrastigma are each monophyletic, and Cayratia may be paraphyletic. Ampelopsis is paraphyletic with the African Rhoicissus and the South American Cissus striata nested within it. The pinnately leaved Ampelopsis form a subclade, and the simple and palmately leaved Ameplopsis constitutes another with both subclades containing Asian and American species. Species of Cissus from Asia and Central America are monophyletic, but the South American C. striata does not group with other Cissus species. The Asian endemic Nothocissus and Pterisanthes form a clade with Asian Ampelocissus, and A. javalensis from Central America is sister to this clade. Vitis is monophyletic and forms a larger clade with Ampelocissus, Pterisanthes, and Nothocissus. The eastern Asian and North American disjunct Parthenocissus forms a clade with Yua austro-orientalis, a species of a small newly recognized genus from China to eastern Himalaya. Vitaceae show complex multiple intercontinental relationships within the northern hemisphere and between northern and southern hemispheres.
Key Words: atpB-rbcL spacer • chloroplast DNA • rps16 intron • trnL-F • phylogeny • Vitaceae
Vitaceae (the grape family) consist of approximately 14 genera and about 900 species (Table 1) primarily distributed in tropical regions in Asia, Africa, Australia, the neotropics, and the Pacific islands, with a few genera in temperate regions (Vitis, Parthenocissus, and Ampelopsis). Ampelopsis and Parthenocissus show a disjunct distribution in eastern Asia and eastern North America extending to Mexico. The family is well known economically for grapes, wine, and raisins (especially Vitis vinifera, as well as several other species and hybrids of Vitis).
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). Most workers have now excluded Leea from Vitaceae and recognized the family Leeaceae (e.g., Planchon, 1887
; Suessenguth, 1953b
; Ridsdale, 1974
; Shetty and Singh, 2000
; Latiff, 2001a
; Ren et al., 2003
; Wen, in press
), although APG (1998)
and APGII (2003)
placed Leea in Vitaceae. Several workers recognized Leea as comprising the subfamily Leeoideae within Vitaceae (see Gilg, 1896
; Gilg and Brandt, 1911
). Vitaceae were usually placed in the order Rhamnales along with Rhamnaceae (e.g., Kirchheimer, 1939
; Cronquist, 1981
, 1988
). Takhtajan (1997)
recognized the order Vitales as consisting of Vitaceae and Leeaceae and considered the Vitales as highly isolated and as a sole member of the superorder Vitanae in the Rosidae. Chase et al. (1993)
reported that the Vitaceae-Leeaceae clade was sister to Dilleniaceae based on rbcL sequence data. The three-gene (atpB, rbcL, and 18S) analysis of Soltis et al. (2000)
placed Vitaceae sister to the rest of the rosids, but did not confirm a close relationship between Vitaceae and Dilleniaceae. APG II (2003)
added Vitaceae to the rosids, but left it unassigned to order.
Vitaceae are usually woody climbers or herbaceous vines or small succulents with leaf-opposed tendrils. These tendrils are considered to be modified shoots or inflorescences (Tucker and Hoefert, 1968
; Gerrath et al., 2001
). Leaves in Vitaceae commonly bear "pearl" glands, and these glands are usually small spherical epidermal structures with a short stalk. Inflorescences of Vitaceae are typically paniculate systems (Troll, 1969
). Flowers of Vitaceae are relatively uniform in morphology at maturity and not particularly informative in systematic studies. Nectary morphology is highly variable in Vitaceae and has been emphasized in defining genera (Suessenguth, 1953a
; Gerrath et al., 2004
). The floral disk is a typical nectariferous, saucer-like structure in Ampelopsis. In Vitis, the disk is morphologically evident at maturity, but is not known to produce nectar. In Parthenocissus, it is not morphologically recognizable, but there is some nectar production. The disk is initiated from the base of the ovary. Externally, the seeds are unusual in comparison with those of other angiosperms in that they have a cordlike raphe on the adaxial surface extending from the hilum to the seed apex and continuing onto the abaxial surface. A groove is commonly present on both sides of the raphe, and a chalazal knot (a depressed to raised region) is on the abaxial surface. The endosperm rumination is highly complex in Vitaceae (Periasamy, 1962
). Detailed systematic vegetative and floral developmental studies have been conducted by Gerrath, Posluszny, and their collaborators (e.g., Gerrath and Posluszny, 1988a
, b, c; 1989a, b, c; Gerrath et al., 1998
, 2001
).
The generic delimitation in Vitaceae has been problematic. Linnaeus (1753)
only recognized two genera: Cissus and Vitis in the family. Hooker (1862)
included Vitis, Pterisanthes, and Leea in the Ampelideae (=Vitaceae), treating Cissus as a synonym of Vitis. Baker (1871)
and Lawson (1875)
followed Hooker in merging Cissus with Vitis. Planchon (1887)
provided a worldwide monograph of the family and defined most genera recognized today. He enumerated 10 genera in Ampelideae (=Vitaceae) and classified Vitis, Ampelocissus, and Cissus into subgeneric groups (sections and series for Vitis and sections for the latter two). Planchon's classification was largely followed by later workers (Viala, 1910
; Suessenguth, 1953a
; Brizicky, 1965
; Latiff, 1982
, 1983
, 2001a
, b; Li, 1998
; Lombardi, 1997
, 2000
; Shetty and Singh, 2000
). Several genera were described subsequently, e.g., Acareosperma (Gagnepain, 1919
), Pterocissus (Urban, 1926
, now treated under the synonymy of Cissus), Cyphostemma (Alston, 1931
), Nothocissus (Latiff, 1982
), and Yua (Li, 1990
). Cyphostemma was included in Cissus by Suessenguth (1953a)
; however, Descoings (1960)
argued for the recognition of Cyphostemma and pointed out the distinctions between the two, especially concerning the bud and corolla shape. The genus has been subsequently recognized by later workers (Mabberley, 1995
; Li, 1998
; Shetty and Singh, 2000
; Latiff, 2001a
). Cissus is characterized by its inflorescence as a leaf-opposite compound cyme, its four-merous flowers, and a continuous cupular floral disk, but was recently shown to be polyphyletic (Rossetto et al., 2002
).
Ingrouille et al. (2002)
sequenced the rbcL gene for 19 species of 10 genera in Vitaceae and one in Leeaceae. They showed that (1) Leeaceae are sister to Vitaceae s. str.; (2) Ampelopsis is basally branching, Cissus, Ampelocissus, and Clematicissus are intermediate, and Vitis most derived; (3) Vitis forms a clade with Cayratia, Cyphostemma, Parthenocissus, and Tetrastigma; (4) Cayratia and Tetrastigma form a weakly supported clade; and (5) Vitis is paraphyletic, and Ampelopsis is polyphyletic.
Rossetto et al. (2002)
investigated 30 species belonging to five genera (Ampelocissus, Cayratia, Cissus, Clematicissus, and Tetrastigma), which mostly included taxa from Australia, a few species of Vitis, and a species of Leea (Leeaceae) using the chloroplast trnL intron and nuclear ribosomal ITS1 sequences. They showed that Cissus is polyphyletic and at least five species should be separated from the genus. Cissus opaca is grouped with Clematicissus, four Australian species (C. antarctica, C. hypoglauca, C. oblonga, and C. sterculiifolia) form a clade with Vitis. Other Cissus species form a large clade. Cayratia is paraphyletic and constitutes a well-supported clade with Tetrastigma.
Phylogenetic analyses with a broader sampling of taxa and markers are needed to further understand the relationships within Vitaceae and test the generic delimitation within the family. Objectives of our paper are to (1) construct the phylogeny of Vitaceae using three chloroplast markers and (2) test the generic delimitations in the family.
MATERIALS AND METHODS
Taxon sampling
A total of 108 accessions representing 79 species of Vitaceae and 12 outgroup taxa were sequenced for the trnL intron and the adjacent trnL-F spacer (Appendix). Our sampling well represents the taxonomic diversity of the family with 12 of the 14 recognized genera included. Only two genera, the monotypic Acareosperma from Laos (Gagnepain, 1919
) and Clematicissus (Jackes, 1989
) from Western Australia, were not sampled. The closely related Leeaceae plus several members of Rhamnaceae and Dilleniaceae were selected as outgroups due to the highly isolated position of the Vitaceae-Leeaceae clade and based on the recent rbcL and 18S data (Chase et al., 1993
; Soltis et al., 2000
).
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DNA extraction, amplification, and sequencing
DNAs of all samples were extracted from silica-gel-dried leaves following a modified CTAB buffer method (Doyle and Doyle, 1987
). Leaves were ground into fine powder with sand at room temperature and incubated with 4x CTAB buffer, with 2% PVP (polyvinyl pyrrolidone), 2% PEG (polyethylene glycol), 1% sodium bisulfite, and 2% 2-mercaptoethanol at 60°C for 120 min. DNA was further purified with SEVAG (24 : 1 chloroform : isoamyl alcohol) twice, and was then precipitated with isopropanol once, followed by precipitation with 5.0 M NaCl and a wash with ethanol and a final precipitation with 3.0 M NaOAc (pH 4.8) and a wash with ethanol.
The trnL intron and trnL-trnF intergenic spacer were amplified using the primers of Taberlet et al. (1991)
. An additional primer, trnL-F f' (5'-ATT TTC AGT CCT CTG CTC TAC C-3'), was designed for Vitaceae because many species failed to get amplified with the primer f (A50272) of Taberlet et al., 1991
. Amplification reactions were performed in a 20-µL volume containing 1.5 mmol/L MgCl2, 0.2 mmol/L of each dNTP, 0.2 µmol/L each primer, 1 U of Taq polymerase, and about 25 ng of DNA temperate. PCR was done on a Peltier Thermal Cycler DNA engine DYAD (MJ Research Incorporated, Watertown, Massachusetts) starting at 94°C for 2 min, followed by 38 cycles of 1 min at 94°C, 1 min at 50°C, 2 min at 72°C, and ended with a final extension of 5 min at 72°C. PCR products were run in agarose gel. The gel containing desired fragments were cut and treated with gelase to digest the gel. Sequencing of both strands was done on an ABI 3100 Genetic Analyzer (Applied Biosytems, Foster City, California, USA) using ABI BigDye version 3.0. PCR profile of sequencing was 25 cycles of 30 s at 96°C, 15 s at 50°C, and 4 min at 60°C. RAMP was set at 1°C/s. The atpB-rbcL spacer and the rps16 intron were amplified and sequenced based on protocols in Bremer et al. (2002)
and Nie et al. (2005)
, respectively. DNA sequences were assembled using SEQUENCHER v3.1 (Gene Codes Corp., Ann Arbor, Michigan, USA). Sequence alignment was initially performed using Clustal X version 1.81 (Thompson et al. 1997
) with the gap-opening penalty set at 10 and the gap extension penalty at 3. Sequence alignments were manually adjusted using BioEdit (Hall, 1999
).
Phylogenetic analyses
Four data sets were analyzed to infer relationships of Vitaceae: (1) a trnL intron and trnL-F spacer matrix of 108 accessions with Leea and Rhamnus as the outgroups; (2) an atpB-rbcL spacer matrix with 28 species of Vitaceae and two species of Leea as the outgroups; (3) a rps16 intron of 32 taxa including two of Leea and one of Dillenia species as the outgroups; and (4) the combined chloroplast data sets with 37 taxa with Leea and Dillenia as the outgroups. In each analysis, all the gaps are treated as new characters, except for ambiguous gaps. Ambiguous gaps were the ones located in regions with tandem repeats of one or a few nucleotides, which may cause difficulties in recognizing homology. Overlapping gaps were treated as independent characters; in that case, the position of smaller gaps was treated as missing data in the accessions possessing larger gaps. Furthermore, phylogenetic analyses with all the gaps treated as missing data were executed for all four data sets. The trees from the analyses with gaps as missing data were congruent with those with gaps treated as new characters, but the resolution was lower.
Parsimony analyses were conducted using PAUP* version 4.0b10 (Swofford, 2003
) with heuristic search, random taxon addition, tree-bisection-reconnection (TBR) branch swapping, and the Mulpars and Steepest descent options. Bootstrap analyses (Felsenstein, 1985
) were performed using 500 replicates, with the random taxon addition sequence limited to 10 and branch swapping limited to 10 000 000 rearrangements per replicate.
Nucleotide substitution model parameters were determined for the cpDNA data sets using MODELTEST version 3.0 (Posada and Crandall, 1998
). A heuristic maximum likelihood search with TBR branch swapping was then conducted. Branches were collapsed (creating polytomies) if the branch length was less than or equal to 1e-08, and the random taxon addition sequence was limited to 100.
Bayesian analyses (Rannala and Yang, 1996
; Mau et al., 1999
) were carried out using MrBayes version 3.0b3 (Huelsenbeck and Ronquist, 2001
) with the model parameters determined from the MODELTEST. Bayesian analyses started from random trees and employed four Markov chain Monte Carlo (mcmc) runs, monitored over one million generations, re-sampling trees every 100 generations. Runs were repeated twice to confirm results. The resulting log likelihood and number of generations were plotted to determine the point after which the log likelihoods had stabilized. After discarding the trees saved prior to this point as burn-in, the remaining trees were imported into PAUP* and a 50% majority-rule consensus tree was produced to obtain posterior probabilities of the clades.
RESULTS
The characteristics of the sequences are shown in Table 2. The aligned positions of the trnL-F, atpB-rbcL, and rps16 intron data sets are 1189, 1050, and 1025 bp, respectively. The phylogenetically informative sites are 218 in trnL-F, 86 in atpB-rbcL, and 179 in rps16 intron. The insertions-deletions, which are transformed into binary character in the analyses, are 41 in trnL-F, 21 in atpB-rbcL, and 34 in rps16 intron.
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The results of this study revealed several relationships among genera of Vitaceae. They also indicated problems concerning generic delimitations of some genera.
Clade A: the Ampelopsis-Rhoicissus-Cissus striata clade
In all analyses except the trnL-F data, the eastern Asian and eastern North American Ampelopsis, the African Rhoicissus, and the South American Cissus striata are strongly supported to form a monophyletic group. The two species of Rhoicissus form a clade sister to Cissus striata. Ampelopsis is paraphyletic with a recognizable subclade of pinnately leaved species (e.g., A. arborea and A. cantoniensis) and another subclade of simple or palmately leaved species (e.g., A. cordata and A. delavayana) in the combined analysis (BS = 70, PP = 98, Fig. 4). Both subclades include species from eastern Asia and North America, suggesting that intercontinental disjunction has evolved at least twice in this genus. The pinnately leaved group was informally recognized as sect. Leeaceifoliae by Galet (1967)
and the simple or palmately leaved group as sect. Ampelopsis. Bernard (1972–1973)
examined buds in Ampelopsis and found that taxa in sect. Leeaceifoliae (with A. bipinnata Michx = A. arborea, A. chaffanjonni, A. megalophylla, and A. orientalis Planch. examined) had complex axillary buds like Vitis vinifera, whereas those in sect. Ampelopsis (with A. aconitifolia, A. bodinieri, A. brevipedunculata, A. citrulloides Lebaas, A. delavayana, A. heterophylla (Thunb.) Sieb. & Zucc. = A. glandulosa, and A. micans Rehder examined) all had serial accessory buds (J. Gerrath, University of Northern Iowa, personal communication). Both morphological and phylogenetic data suggest that Ampelopsis needs to be redefined and the "Leeaceifoliae" group may need to be raised to the generic rank.
Geographically, this Ampelopsis-Rhoicissus-Cissus striata clade (clade A, Fig. 4) demonstrates an unusual distributional pattern. Most species of Ampelopsis are distributed in Asia and three species in North and Central America. Rhoicissus is an endemic genus to Africa with about 12 species, and Cissus striata is from South America. Although about 75 species of Cissus are known in South and Central America, only three (C. palmata, C. striata, and C. sulcicaulis) have their distribution range extending into the southern part of South America (Lombardi, 2000
). Within the distributional area of Cissus striata, there are other South American-Asian disjunct plants such as Lardizabalaceae, Hydrangea, and Berberis (Good, 1974
), as well as South American-African disjuncts (Goldblatt, 1995
). This biogeographic relationship observed in Vitaceae clearly needs to be further explored with additional sampling in Cissus especially the taxa from Africa, Australia, and South America.
Clade C-1: the Ampelocissus-Nothocissus-Pterisanthes clade
Within clade C (Fig. 4), Ampelocissus, with A. javalensis from Central America excepted, Nothocissus, and Pterisanthes form a clade (BS = 92, PP = 100) in the combined tree. Nothocissus is a small Asian genus with five species distributed in Malaysia, Indonesia, and Papua New Guinea (Latiff, 1982
; 2001a
, b). It is a poorly defined genus, and its generic status needs to be critically examined. Pterisanthes is also an Asian genus with about 20 species distributed in Malaysia, Indonesia, Philippines, and Thailand (Wen, in press
). Species of Pterisanthes are characterized by their leaf-opposed applanate or lamellate panicle with branched tendrils on the peduncle. Ampelocissus is a relatively large genus with c. 90 species distributed in Asia, Africa, and North and South America. Our results suggest that Asian Ampelocissus is more closely related to Pterisanthes and Nothocissus than to its congeneric species in Central America.
Ampelocissus is characterized by its 4–5-merous flowers in thyrses and inflorescences subtended by a tendril near the base. All species of Ampelocissus sampled in this study are from Asia except for A. javalensis, which represents one of the four New World species. Ampelocissus javalensis is sister to the clade of Asian Ampelocissus, Nothocissus, and Pterisanthes. This position is congruent with those of the trees of trnL-F and atpB-rbcL. This is a closely related and morphologically diverse clade showing geographic integrity. On the other hand, Ampelocissus martinii of southeast Asia, is separated from the other Asian Ampelocissus. Its taxonomic position needs to be reexamined with more taxa of the genus sampled. Our phylogenetic data clearly suggest the problematic generic circumscription of Ampelocissus.
Clade C-2: monophyly of Vitis
Within clade C, the Asian and North American Vitis species form a clade. Vitis is strongly supported as a monophyletic group in all analyses. Based on the rbcL data, Ingrouille et al. (2002)
have, however, reported that Vitis is paraphyletic with Cyphostemma and Parthenocissus nested within it, but this relationship has no bootstrap support. In the present study, Vitis is monophyletic and forms a clade with Ampelocissus, Pterisanthes, and Nothocissus (BS = 91, PP = 100) (Fig. 4). Furthermore, the large Vitis-Ampelocissus-Nothocissus-Pterisanthes clade (clade C) is sister to the clade of Parthenocissus and Yua austro-orientalis (clade B).
Species of Vitis are morphologically characterized by their polygamodioecious reproductive biology, calyptrate petals, and five-merous flowers. Two subgenera are commonly recognized in the genus: subg. Vitis and subg. Muscadinia. Species of subg. Vitis usually have shreddy bark on old stems, lenticels inconspicuous (vs. prominent in subg. Muscadinia), pith interrupted by diaphragms within the nodes (vs. continuous through nodes in subg. Muscadinia), and tendrils 2–3-forked (vs. simple in subg. Muscadinia). Subgenus Muscadinia consists of only 2–3 species from the USA, the West Indies, and Mexico (Brizicky, 1965
), whereas subg. Vitis has a wide distribution in the northern hemisphere. We sampled V. arizonica and V. rotundifolia of subg. Muscadinia and the other species belonging to subg. Vitis. With our present data, we cannot evaluate this infrageneric classification of Vitis due to our limited taxon sampling in this genus.
Clade E: the Cayratia-Cyphostemma-Tetrastigma clade
The three genera, Cayratia, Cyphostemma, and Tetrastigma form a strongly supported clade in all trees (Figs. 1–4). Within the clade, Cyphostemma and Tetrastigma are each monophyletic, but Cayratia is paraphyletic except in the rps16 tree (cf. Figs. 1– 4). Cayratia is distributed in tropical-subtropical regions in Asia, Africa, Australia, and Pacific Islands (Jackes, 1987
). Within Cayratia, a close relationship between C. japonica and C. trifolia is suggested based on morphology (Latiff, 1983
) and molecular ITS data (Rossetto et al., 2002
). One of the two Cayratia clades in the trnL-F tree includes both C. japonica and C. trifolia (BS = 99, PP = 100, Fig. 1), supporting their close affinity.
The clade of Cayratia and Tetrastigma has been reported by previous studies (e.g., Ingrouille et al., 2002
; Rossetto et al., 2002
). Our study supports their results, but the position of Cyphostemma is different in these analyses. In the rbcL tree, Cyphostemma juttae is in a clade with Vitis and Parthenocissus, which is then sister to the Cayratia and Tetrastigma clade (Ingrouille et al., 2002
). Our analyses from all three chloroplast markers, however, strongly support the clade of Cayratia, Cyphostemma, and Tetrastigma (clade E).
Alston (1931)
raised Cissus sect. Cyphostemma Planch. to the generic rank. Cyphostemma was, however, treated as a synonym of Cissus by Suessenguth (1953a)
. Descoings (1960)
argued for the separation of Cyphostemma from Cissus and recognized the genus in several floristic treatments in Africa (e.g., Descoings, 1967a
, b, 1975). Cyphostemma has been accepted recently by several workers (e.g., Mabberley, 1995
; Shetty and Singh, 2000
; Latiff, 2001a
; Wen, in press
). Although only three of the approximately 200 species of this genus are included in this study, Cyphostemma is shown to be distinct from the polyphyletic Cissus (Figs. 1– 4; also see Rossetto et al., 2002
). Morphologically, Cyphostemma is characterized by its unique flask-shaped floral buds and its floral disk of four free glands (Descoings, 1960
). The morphological synapomorphies of the strongly supported Cayratia-Cyphostemma-Tetrastigma clade need to be documented.
Clade B: Parthenocissus and Yua
Parthenocissus forms a clade with Yua austro-orientalis in the combined tree (BS = 76). Yua was recently established by Li (1990)
and includes three species from central and South China, Nepal, and northern India. Taxa of Yua were previously included in Parthenocissus (Planchon, 1887
; Rehder, 1945
). Li (1990)
argued that species of Yua differed in their tendril and inflorescence morphology and should be separated as a distinct genus. Yua possesses bifurcate (vs. 3-12 branched in Parthenocissus) tendrils and leaf-opposed (vs. terminal or nearly so in Parthenocissus) inflorescence. Morphologically, the digitate leaf form, the fall color change of leaves from green to red, the five-merous flower, and the inconspicuous floral discs of Yua support its close relationship with Parthenocissus (Wen, in press
). The generic status of Yua still needs further evaluation with additional sequence data of other congeneric species.
Clade D: Cissus
Two groups were recognized within the 13 species of Cissus analyzed in our study, one consisting of C. striata, and the other composed of taxa from Asia and Central America (clade D in Fig. 4). Cissus is a large genus with about 350 species distributed throughout the tropics. It has remarkable morphological diversity (Jackes, 1988
). Rossetto et al. (2001
, 2002
) have recently shown that Cissus is polyphyletic using chloroplast trnL intron and nuclear ribosomal ITS sequences. Our study also supports that Cissus is at least biphyletic based on our sampling alone. Our study also shows that the South American C. striata occupies an unusual position in Vitaceae. It is supported to be closely related to the African Rhoicissus, and the Asian-North American disjunct Ampelopsis. A broader sampling is required to further test this relationship.
Conclusions
Phylogenetic analyses of 12 genera and 79 species of Vitaceae provided a fairly well-supported phylogeny of the family. The trnL-trnF tree alone was poorly resolved concerning intergeneric relationships. When two additional chloroplast markers, atpB-rbcL spacer and the rps16 intron, were included, much higher resolution was obtained. Several closely relationships between genera are suggested: Ampelopsis, Rhoicissus, and Cissus striata in clade A; Yua and Parthenocissus in clade B; Ampelocissus, Nothocissus, Pterisanthes, and Vitis in clade C; Cayratia, Cyphostemma, and Tetrastigma in clade E. Within clade C, Vitis forms a subclade (C2). Ampelopsis and Parthenocissus each demonstrate an Asian-New World disjunct distribution, suggesting multiple intercontinental migrations in this family. Furthermore, The clade of the Asia-North American Ampelopsis, South American Cissus striata, and African Rhoicissus shows an unusual biogeographical relationship among Asia, North and South America, and Africa. The Cayratia-Cyphostemma-Tetrastigma clade have a close biogeographic relationship of southeastern Asia, Australia, and Africa including Madagascar. Vitaceae thus have complex multiple intercontinental relationships within the northern hemisphere and between northern and southern hemispheres.
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This study was supported by grants from the U.S. National Science Foundation (DEB0108536) and the Institute of Botany, the Chinese Academy of Science (to J.W.), the Pritzker Laboratory for Molecular Systematics and Evolution of the Field Museum, a Bass Fellowship from The Field Museum, and Smithsonian Institution research funds (to A.S.). The authors thank J. Gerrath for sending plant material and providing helpful advice and two anonymous reviewers for constructive comments. 
4 Author for correspondence (e-mail: wenj{at}si.edu
)
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