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Systematic Botany (2001), 26(1): pp. 144–167 ᭧ Copyright 2001 by the American Society of Plant Taxonomists

The Evolution of Araliaceae: A Phylogenetic Analysis Based on ITS Sequences of Nuclear Ribosomal DNA

JUN WEN Department of Biology, Colorado State University, Fort Collins, Colorado 80523 Current address: Department of Botany, Field Museum of Natural History, Roosevelt Rd at Lake Shore Dr., Chicago, Illinois 60605-2496

GREGORY M. PLUNKETT Department of Biology, Virginia Commonwealth University, Richmond, Virginia 23284-2012

ANTHONY D. MITCHELL Ecology and Entomology Group, Soil, Plant and Ecological Sciences Division, PO Box 84, Lincoln University, Canterbury, New Zealand

STEVEN J. WAGSTAFF Landcare Research, P.O. Box 69, Lincoln 8152, New Zealand

Communicating Editor: Alan Whittemore

ABSTRACT. Phylogenetic analyses of ITS sequence data from 70 species and 40 genera of Araliaceae (representing all major lineages within the ‘‘core group’’ of the family) do not support the widely used traditional division of Araliaceae into three tribes. Tribe Aralieae (characterized by imbricate petals) is found nested within a paraphyletic Schefflerieae (whose taxa have valvate petals). There are, however, two large monophyletic groups comprising most araliad genera: the ’’Aralia-Polyscias-Pseudopanax group’’ (which in- cludes Aralia, Meryta, Munroidendron, Panax, Pentapanax, Polyscias, Pseudopanax, Reynoldsia, Sciadodendron, Tetra- plasandra, and their close allies), and the ’’Eleutherococcus-Dendropanax-Schefflera group’’ (including Brassaiopsis, Dendropanax, Eleutherococcus, Fatsia, Hedera, Oreopanax, Schefflera, Sinopanax, and their close allies). The ITS trees also permit a re-evaluation of several taxonomically important morphological characters (e.g., petal aestivation, leaf architecture, carpel number, and habit), and provide the opportunity to assess traditional generic delimitations in the family. Four of the largest genera appear to be either polyphyletic (Schefflera, Pseudopanax) or paraphyletic (Aralia, Polyscias), but further studies will be needed to fully re-define these complex taxa. Outgroup comparisons and the placement of Astrotricha and Osmoxylon (in basally-branching lineages in Araliaceae) help to confirm a paleotropical origin of the family. The ITS topologies suggest that biogeographic radiations into different tropical/subtropical regions and into the north and south temperate regions occurred early in the history of core Araliaceae. Temperate taxa have arisen several times indepen- dently from tropical and subtropical relatives, although a few subtropical taxa may be found nested within temperate clades (e.g., Pentapanax within Aralia). Migrations between the Old and New Worlds are also sug- gested for several taxa, including Aralia, Panax, Oplopanax, and the Sinopanax—Oreopanax generic pair.

Araliaceae (the ginseng family) comprise approx- traditionally been allied with Apiaceae on the basis imately 55 genera and 1,500 species. The family is of morphological (Harms 1898; Judd et al. 1994) most broadly distributed in the tropics and sub- and anatomical evidence (Metcalfe and Chalk tropics (especially in southeastern and southern 1950), and this treatment has been largely support- Asia and the Pacific islands), but there are several ed by recent molecular studies (Plunkett et al. well-known genera from the temperate zones as 1996a, 1997). Most systems of classification place well (e.g., Aralia, Hedera, Oplopanax, and Panax). The Araliaceae and Apiaceae together in the order Api- family includes a number of important medicinal ales (sensu Cronquist 1981, 1988; or its taxonomic plants, such as Panax (ginseng) and Eleutherococcus equivalent, Thorne 1992; Takhtajan 1987, 1997), (Siberian ginseng), and several well-known orna- which in turn has been placed in or near subclass mentals, including Hedera (English ivy), Schefflera Rosidae (e.g., Cronquist 1981, 1988). Recent studies, (the umbrella trees), and Polyscias. Araliaceae have however, suggest that Apiales should be placed in

144 2001] WEN ET AL.: ARALIACEAE EVOLUTION 145 a broadly defined Asteridae (Chase et al. 1993; later workers as ‘‘artificial’’ due to its heavy reliance Olmstead et al. 1993; Plunkett et al. 1996a; Soltis et on inflorescence characters (see Hoo and Tseng al. 1997) closely allied to Pittosporaceae (Plunkett 1978; Frodin 1982; Tseng and Hoo 1982; Wen 1991, et al. 1996a, 1997; Xiang and Soltis 1998). 1993; Wen et al. 1998). In fact, inflorescence struc- Araliaceae are characterized by relatively con- ture may be variable within a single genus (e.g., served floral, but diverse vegetative features (Phi- Aralia, Wen 1991, 1993; Schefflera, Frodin 1982) or lipson 1970a; Eyde and Tseng 1971). Members of even within a single section (e.g., Aralia sect. Aralia, the family possess five sepals, 5–10 (–12) petals, Wen et al. 1998). Tseng and Hoo (1982) proposed a which are free or form a calyptra (as in Pentapanax system of five tribes: Aralieae, Panaceae, Pleran- and Tupidanthus), mostly 5–10 stamens (rarely to dreae, Tetraplasandreae, and Mackinlayeae. Their numerous, e.g., 120 in Tupidanthus), and a gynoeci- system is largely a refinement of Harms’ (1898) um with 2–10 (mostly 5, rarely up to 200 in Tupi- treatment with a greater emphasis on leaf architec- danthus, or1inSeemannaralia R. Viguier) locules, ture. They divided Harms’ Aralieae into two tribes: and an inferior ovary (rarely superior as in Dipanax Aralieae s. str., with leaves once to several-times Seem.) with a nectary disk. Most araliads produce pinnately compound, and Panaceae, with simple or berries or drupaceous fruits that are bird dispersed palmately compound leaves. They also divided (Ridley 1930). The leaves of Araliaceae vary from Harms’ Schefflereae into Plerandreae (with simple simple, to variously lobed or divided, to palmately or palmately compound leaves) and Tetraplasan- and/or pinnately compound. Although most spe- dreae (with pinnately compound leaves). cies are trees, shrubs, or woody climbers, there are Although Araliaceae lack a modern systematic also a few herbaceous perennials (e.g., some species treatment, data are available from a wide range of of Aralia and Panax). taxonomic sources. Floristic studies have helped to The major classification systems of Araliaceae in- enumerate the species of Araliaceae from many re- clude those by Bentham and Hooker (1867), See- gions [e.g., China (Franchet 1896; Li 1942; Hoo and mann (1868), Harms (1898), Hutchinson (1967), and Tseng 1978; Shang 1985a), East Africa (Tennant Tseng and Hoo (1982). Bentham (1867) recognized 1968), Europe (Webb 1968; Stace 1993), Hawaii five ‘‘series’’ (ϭ tribes) within Araliaceae based on (Lowry 1986), Japan (Ohwi 1984), Korea (Lee 1993), petal aestivation (imbricate vs. valvate), pedicel Malesia (i.e., Indonesia, Malaysia, and the Philip- type (articulate vs. continuous), breeding system pines, Philipson 1979), New Zealand (Allan 1961), (hermaphrodite, polygamo-dioecious, or dioecious), North America (Smith 1944), the former U.S.S.R. stamen number, and albumen type (ruminate vs. (Poyarkova 1973), and Vietnam (Ha 1974; Hoˆ uniform). Seemann (1868) defined the segregate 1993)]. Further, revisionary treatments have been ‘‘order’’ (ϭ family) Hederaceae as distinct from a completed for several genera [e.g., Aralia (Wen more narrowly circumscribed Araliaceae. His Hed- 1991), Delarbrea (Lowry 1986), Eleutherococcus (Kim eraceae was divided into five tribes (Cussonieae, 1997), Macropanax (Shang 1983), and Schefflera (Fro- Horsfieldieae, Hedereae, Pseudopanaceae, and Pler- din 1975, 1986, 1989; Shang 1984)], and phyloge- andreae), and included all araliads having valvate netic analyses have also been performed for Aralia petals and fruits with two or more carpels. As such, (Wen 1991; Tseng et al. 1993; Wen et al. 1996; Wen it included the vast majority of araliaceous genera, et al. 1998; Wen 1999b), Eleutheroccocus (Kim 1997), excluding only genera with imbricate petals (e.g., Hedera (Vargas 1999), Panax (Wen and Zimmer Aralia and Panax). Harms’ (1898) treatment, which 1996), and Pseudopanax (Mitchell and Wagstaff remains the most widely used (e.g., in Poyarkova 1997). Cytological work has demonstrated that a ba- 1973; Hoo and Tseng 1978; Philipson 1979; Shang sic chromosome number of x ϭ 12 is highly con- 1985a; Mabberly 1997), divides Araliaceae into served throughout the family, with diploid num- three tribes (Aralieae, Mackinlayeae, and Scheffler- bers mostly of 2n ϭ 24 or 2n ϭ 48 (Matsuura and eae) based largely on petal aestivation. Most araliad Suto 1935; Sugiura 1936; Rattenbury 1957; Harn genera, having valvate petals, were placed in tribe and Whang 1963; Graham 1966; Lo¨ve and Ritchie Schefflereae (36 genera), leaving relatively few gen- 1966; Sokolovskaya 1966; Wardle 1968; Stone and era in tribes Aralieae (11 genera) and Mackinlayeae Loo 1969; Hara 1970; Guha 1971; Javurkova 1981; (three genera) (see Table 1). Hutchinson (1967) rec- Yang 1981; Lo¨ve and Lo¨ve 1982; Beuzenberg and ognized seven tribes (Cussonieae, Anomopanaceae, Hair 1983; Starodubtsev 1985; Sun et al. 1988); Plerandreae, Aralieae, Mackinlayeae, Panaceae, and some taxa from Hedera, however, have a diploid Hedereae), but his system was widely criticized by number as high as 2n ϭ 192 (Stace 1993; Vargas 146 SYSTEMATIC BOTANY [Volume 26

TABLE 1. The classification of Araliaceae according to Harms (1898). Modern synonymies are noted in parentheses (‘‘ϭ’’ denotes synonyms in general use; ‘‘cf.’’ denotes synonyms used only in some treatments). Taxa currently excluded from core Araliaceae (sensu Plunkett et al. 1997) are marked with an asterisk (*).

Tribe Schefflereae Tribe Aralieae *Tribe Mackinlayeae Acanthopanax Miq. (ϭ Eleutherococcus Maxim.) Aralia L. *Apiopetalum Baill. Arthrophyllum Blume *Aralidium Miq. *Mackinlaya F. Muell. Astrotricha DC. *Delarbrea Vieill. *Pseudosciadium Baill. Boerlagiodendron Harms (ϭ Osmoxylon) Horsefieldia (ϭHarmsiopanax) Brassaiopsis Decne. & Planch. Motherwellia F. Muell. Cheirodendron Nutt. ex Seem. *Myodocarpus Brongn. & Gris. Crepinella Marchal (cf. Schefflera) Panax L. Cussonia Thunb. Pentapanax Seem. Didymopanax Decne. & Planch. (cf. Schefflera) *Porospermum F. Muell. (ϭDelarbrea) Dizygotheca N. E. Brown (cf. Schefflera) Sciadodendron Griseb. Echniopanax Decne. & Planch. (ϭOplopanax) *Stilbocarpa (Hook. f) Decne. & Eremopanax Baill. (ϭArthrophyllum) Planch. Fatsia Decne. & Planch. Gamblea C. B. Clarke Gastonia Comm. ex Lam. Hedera L. Hederopsis C. B. Clarke (ϭMacropanax) Heteropanax Seem. Kalopanax Miq. Kissodendron Seem. (ϭPolyscias) Macropanax Miq. Meryta Forster & Forster f. Nothopanax Seem. (ϭPolyscias) Oreopanax Decne. & Planch. Osmoxylon Miq. Plerandra A. Gray Polyscias Forster & Forster f. Pseudopanax K. Koch Pterotropia Hillebrand Reynoldsia A. Gray Schefflera Forster & Forster f. Sciadopanax Seem. (ϭPolyscias) Tetrapanax (K. Koch) K. Koch Tetraplasandra A. Gray Trevesia Vis. Tupidanthus Hook. f. & Thoms (cf. Schefflera)

1999). Pollen morphology (Erdtman 1966; Tseng Ducamp 1902; Singh 1954) and the breeding sys- 1971, 1973, 1974; Tseng and Shoup 1978; Tseng et tems have been documented for Aralia (Barrett and al. 1983; Shoup and Tseng 1977; Shang and Callen Helenurm 1981; Thomson and Barrett 1981; Barrett 1988; Park and Lee 1989; Henwood 1991; Wen and and Thomson 1982; Bawa et al. 1982; Flanagan and Nowicke 1999) and wood anatomical features (Vi- Moser 1985), Panax (Hara 1970; Schlessman 1985, guier 1906, 1909; Metcalfe and Chalk 1950; Rodri- 1987, 1990, 1991) and many New Caledonian taxa guez 1957; Oskolski 1994, 1995, 1996; Oskolski et of the family (Schlessman et al. 1990a, b). al. 1997; Oskolski and Lowry 2000) have been ex- More recently, DNA sequencing studies based on amined from many araliad taxa, and secondary the chloroplast genes rbcL and matK (Plunkett et al. chemistry from a few genera has also been reported 1996a, 1997) have provided important insights into (e.g., Ng and Walker 1975; Zhou et al. 1975; Lutom- the evolution and diversification of Araliaceae and ski and Nham 1977; Hansen and Boll 1986). The its relationships with Apiaceae and other closely re- embryology of a few taxa has been published (e.g., lated families. These studies resolved a monophy- 2001] WEN ET AL.: ARALIACEAE EVOLUTION 147 letic group comprising most araliad genera (a clade quences representing taxa of Araliaceae and three referred to as ‘‘core Araliaceae’’), but this core outgroups, table 2). Of these, 45 sequences were group appears to exclude Delarbrea, Mackinlaya, and newly-derived and the remaining 28 were previ- their presumed close relatives (Apiopetalum, Myodo- ously published (marked with asterisks in Table 2, carpus, and Pseudosciadium). Because Plunkett et al. and obtained from GenBank). This sample includes (1996a, 1997) focused on higher-level relationships representatives of most genera of core Araliaceae, throughout the order, the number of araliaceous as well as two or more species from large genera taxa sampled was small, and the relatively con- such as Aralia, Dendropanax Decne & Planchon, served rbcL and matK sequences provided only lim- Eletheroccocus, Polyscias, Pseudopanax, and Schefflera. ited resolution at the intergeneric level in core Ar- Because Araliaceae have traditionally been allied to aliaceae. Thus, no comprehensive study of relation- Apiaceae (Harms 1898; Thorne 1973, 1992; Cron- ships among and within the genera of Araliaceae quist 1981; Judd et al. 1994; Plunkett et al. 1996a, is presently available. Furthermore, many studies 1997), and because recent molecular data suggest a over the past three decades have proposed the re- close relationship of Apiales to Pittosporaceae (e.g., circumscription of araliad genera, but a unified Plunkett et al. 1996a, 1997; Xiang and Soltis 1998), concept of generic delimitation has not been em- Daucus carrota and Hydrocotyle vulgaris of Apiaceae ployed. For example, the definitions of several large and Pittosporum dallii of Pittosporaceae were includ- genera such as Aralia (Wen 1993), Polyscias (Philip- ed as outgroup taxa. son 1979; Lowry et al. 1989), Pseudopanax (Philipson Total DNAs were extracted using the CTAB 1965), and Schefflera (Frodin 1975; Lowry et al. 1989) method of Doyle and Doyle (1987). DNA amplifi- have been broadened, and consequently many cations followed the protocol of Wen and Zimmer smaller genera have been taxonomically sub- (1996), and the sequencing strategy of the entire ITS merged. In contrast, other studies have segregated regions (ITS1 and ITS2) and the 5.8S gene followed smaller genera out of larger ones, including Chen- Wen et al. (1998) or Plunkett et al. (in press). After giopanax Shang & J. Y. Huang from Eleutherococcus manually assembling the DNA sequences, the (Shang and Huang 1993), Evodiopanax (Harms) Na- boundaries between the coding and spacer regions kai from Eleutherococcus (Nakai 1924; Ohashi were determined by comparisons with the previ- 1987b), Metapanax Frodin ex J. Wen & Frodin from ously published ITS sequences of carrot (Daucus car- Nothopanax Miq. (Wen and Frodin, in press), and ota; Yokota et al. 1989). All newly-derived sequences Raukaua Seem. from Pseudopanax (Mitchell et al. have been deposited at GenBank (see Table 2 for 1997). It is necessary, therefore, to re-evaluate ge- accession numbers). Because most mutations were neric concepts in Araliaceae using a phylogenetic base substitutions, manual alignment was straight- framework. forward. To examine evolutionary relationships among the Phylogenetic analyses were performed with genera of core Araliaceae, we have analyzed ITS PAUP* (version 4.0, Swofford 1999) using maxi- sequence data from representatives throughout the mum parsimony (Swofford et al. 1996), maximum family. Phylogenetic analysis of the internal tran- likelihood (Felsenstein 1981), and neighbor-joining scribed spacers of nuclear ribosomal DNA has been (Saitou and Nei 1987) methods in which alignment successfully applied to several intra- and interge- gaps were treated as missing data or as new char- neric problems in Araliaceae (e.g., Wen and Zimmer acters. The maximum parsimony (MP) analysis was 1996; Mitchell and Wagstaff 1997; Wen et al. 1998), performed using a heuristic search with MULPARS and in the closely related family Apiaceae (e.g., and furthest-addition sequence options. Both Fitch Downie et al. 1998; Katz-Downie et al. 1999), as and weighted parsimony analyses were employed. well as many other plant groups (see Baldwin et al. The latter weighted transversions over transitions 1995 for a review). On the basis of ITS data from 1.8 times based on the observed ratio. Decay values Araliaceae, we herein re-evaluate the traditional (Bremer 1988) were calculated by using a reverse classification systems, test the generic limits of sev- constraint and comparing the length differences to eral key araliaceous genera, and examine biogeo- the maximally parsimonious trees (MPTs). The graphic relationships within the family. amount of support for monophyletic groups re- vealed in the maximally parsimonious tree(s) MATERIALS AND METHODS (MPTs) was also examined with 1,000 bootstrap Seventy-three ITS sequences, representing 43 replicates (Felsenstein 1985) with 100 trees saved genera, were analyzed for the present study (70 se- for each due to the large size of the data set. The 148 SYSTEMATIC BOTANY [Volume 26 GenBank accession AF242239 U63184 AF242251 AF229762 AF242252 U63183 AF242240 AF242235 U66704 AF242256 U66925 AF242230 U41675 X17534 AF077895 rsity of Tokyo AF242238 rsity of Tokyo AF242234 rsity of Tokyo AF242245 Geographical origin Cult. in Fort Collins, CO Jilin, China Royal Botanic Gardens, Kew Cult. in Botanical Gar den, Unive Queensland, Australia Maui, Hawaii Yunnan, China Hainan, China Connecticut, USA Arizona, USA Kentucky, USA (CHR) (CHR 500673) New Zealand U63196 (A) Decatur Co., GA U66928 (CHR 452093) NSW, Australia U63189 Voucher (MO) (WS) Africa AF229765 (MO) Madagascar AF229737 (CHR 484172) NSW, Australia U63190 (CS) (CS) Sichuan, China AF242250 (CS) (CS) (CS) Yunnan, China AF242227 (CS) Cult. in Botanical Gar den, Unive (CS) (CS) Cult. in Botanical Gar den, Unive (CS) (CS) (CS) (A) (CHR 502518) Riviere Bleue, New Caledonia U63182 (OS) Baja California, Mexico U66927 (SYS) Cult. in South Cina Bot. Gard. AF242237 (SYS) Cult. in South China Bot. Gard. AF242236 G.M. Plunkett 1519 J. Wen 3092 J. Wen 2488 Plant 1976-6252 J. Wen 3112 J. Wen 1150 T.G. Lammers & R. Holody Lowry 5677 P.P. 5013 S. Shi 001 J. Wen 2461 J. Wen 2476 G.M. Plunkett 1341 S. Shi 002 B.J. Lepschi 666 J. Wen 2477 R. O. Makinson 592M W. Lee s.n. J. Wen & H. Dong 976 J. Wen 1149 J. Wen 1136 T. Philbrick s.n. J. Wen 4974 J. Wen 1071 J. Wen 565 V. Gamble & N. W. Nelson s.n. (W. W. Sm.) S. Y. Hu (Baill.) Philipson Species (Rupr. & Maxim.) S. Y. Hu R. Viguier & Guillaumin (Merr. & Chun) Chun (Gaud.) A Heller Schneid. Decne. & Planchon (Champ.) Benth. (Thunb.) Makino Endl. (Roxb.) Hutch D.C. Benth. Brandg. Cheesem. (Pittosporaceae) Clarke L. Thunb. L. Hand.–Mazz. L. L. (Apiaceae) Vent. DC. 2. Names, sources, and GenBank accession numbers of the 45 newly derived and 28 previously published (marked with ‘‘*’’) ITS sequences from Araliaceae and ABLE T Eleutherocococcus nodiflorus Cheirodendron trigynum Astrotricha ledifolia Astrotricha latifolia Aralia spinosa Arth rophyllum angustatum Aralia hispida Aralia racemosa Aralia scopulorum Daucus carota Pittosporum dallii Aralia apioides Eleutherococcus simonii Euaraliopsis palmata Dendropanax trifidus Dizygotheca elegantissima * Eleutherococcus sessiliflorus Cussonia spicata Cephalaralia cephalobotrys * Cuphocarpus aculeatus Dendropanax hainanensis Dendropanax proteus Brassaiopsis mitis Brassaia actinophylla * * * * Aralia chinensis * Aralia humilis * * three outgroup taxa. Herbarium acronym follows Holmgren et al. (1990). Outgroup * * *Hydrocotyle vulgaris L. (Apiaceae) Araliaceae * 2001] WEN ET AL.: ARALIACEAE EVOLUTION 149 GenBank accession AF242249 AF242254 Geographical origin field, OH Yunnan, China AF242253 Cult. in RBG Kew, Acc# 1913-5202 U63187 2. Continued. Voucher ABLE (WS) Cult. in MoBG 850020 AF229738 (MO) New Guinea AF229727 (MO)(MO) Queensland, Australia Queensland, Australia AF229688 AF229705 T (CHR) Cook Islands U63195 (CHR) Cult. in Otago, New Zealand U63186 (MO) New Caledonia AF229701 (MO) New Caledonia AF229717 (MO) Vietnam AF229767 (MO) Vietnam AF229766 (CHR 502421) Christchurch Botanical Garden native section U63177 (CHR 500663) Cult. in Lincoln, New Zealand U63165 (CHR 500662) Cult. Christchurch, New Zealand U63194 (CHR 502463) Cultivated in Halswell, New Zealand U63193 (CS) Cult. in Mexico City, Mexico AF242229 (CS) Mans (CHR 500668) Arthurs Pass, New Zealand U63178 (CHR 500669) Chatham Islands U63166 (CS) Heilongjiang, China U41680 (CS) Yunnan, CHina AF242255 (CS) Yunnan, China AF242232 (CS) Hubei, China AF242233 (CS)(CS) Cult. in Fort Collins, CO Cult. in South Bot. Garden AF242241 AF242242 (CS) Yunnan, China AF242228 (CS) Cult. Nikko Botanical Garden AF242248 (CS) Cult. in Fort Collins, Co AF242246 D. Kramer s.n. B. Molley s.n. A. Mitchell s.n. J. Wen 68 LowryP.P. 4754 A. Mitchell s.n. G.M. Plunkett 1342 J. Wen 517 F. Chiang 1278 G.M. Plunkett 1489 J. Wen 1250 Sino-Amer. Bot. Exp. 125 (US) P. Heenan s.n. J. Wen 3017 G.M. Plunkett 1500 G.M. Plunkett 1507 J. Wen 1217 E. H. Wilson 1680 LowryP.P. 4940 W. Sykes 4655/CI A. Mitchell s.n. A. Mitchell s.n. J. Wen 1409 Acc#: 662-86.06150 (RBG Kew)P.N. Johnson 670 J. Wen 2481 J. Wen 2213 Rodrigues, Mauritius (cultivated at Kew) AF229723 J. Wen 3050 Species (C.N. Forbes) Sherff Kirk Becc. (Franch.) Nakai (Bl.) Ktze. (Murr.) Philipson (Hook. f.) C. Koch (DC.) C. Koch (Roxb.) Seem. (Li) Shang Seem. (Nakai) Nakai (F. v.M.) Philipson (Schlechtd.) Decne. (Franch.) Frodin ex J. Wen & Frodin Harms Acc#: 1547/86 Christchurch Botanical Gardens, New Zealand U63191 (Bull.) L. H. Bailey Hemsl. ex Cheesem. (Franch.) Frodin ex J. Wen & Frodin (Thunb.) Nakai (Hook. f.) Seem. iofolius (R. Viguier) Lowry guinaensis (Scheff.) Becc. Acc#: 810791002 (Nat’l Tropical Botanical Garden) New Guinea AF229726 L. C.A. Meyer (Thunb.) Decne & Planch. (Benth.) Harms L. L. anax fragrans Panax ginseng Panax trifolius Pseudopanax linearis Pseudopanax lessonii Pseudopanax chathamicus Polyscias fruticosa Pseudopanax arboreus Meryta sinclairii Meryta pauciflora Hedera helix Kalopanax pictus Fatsia japonica Polyscias lecardii Oplopanax japonicus * Oreopanax echinops Osmoxylon geelvinkianum Osmoxylon novo- * Pentapanx racemosus * Pentapanax plumosus * Polyscias mollis * Polyscias guilfoylei Polyscias australiana * Polyscias sessiliflora Lowry P.P. 4981 * Munroidendron racemosum Macropanax dispermus * Metapanax delavayi * Metapanax davidii * Hedera helix Heterop * Gamblea pseudoevodiaefoliaGastonia rodriguesensis Lowry P.P. 4856 Evodiopanax evod * 150 SYSTEMATIC BOTANY [Volume 26

maximum likelihood (ML) analysis was performed with the input order of sequences randomized and the transition/transversion ratio set at 1.8. A neigh- GenBank accession bor-joining (NJ) tree was constructed using the Ki- mura two-parameter distance (Kimura 1980).

apan AF242243 RESULTS

Characteristics of ITS Sequences of Araliaceae. The combined length of the entire ITS region (ITS1, 5.8S, and ITS2) from taxa sampled throughout Ar- aliaceae ranged from 600 to 612 bp. The ITS1 region was 218–224 bp in length, the 5.8S gene was 164– 166 bp, and the ITS2 region was 215–224 bp. Thirty- Geographical origin two insertions or deletions (indels) were necessary to align the 72 sequences. Of these, 21 indels were located in the ITS1 region, two in the 5.8S gene, and nine in the ITS2 region. The indels ranged in length from 1 to 8 bp, but most were only 1–2 bp long and represented autapomorphies. The single 8-bp indel was a synapomorphic deletion detected in the ITS2 region of the two species of Osmoxylon Miq. Little length variation was observed in the 5.8S region, which was 164 bp long in 68 of the 73 sequences. Alignment of the sequences yielded a data matrix of 720 total characters, of which 248 were poten- tially parsimony informative. Treating gaps as 2. Continued. missing data, the Kimura two-parameter distances Voucher ABLE (WS) Hawaii AF229740 (WS) Hawaii AF229739 (WS)ranged from 0.663–20.724% Cultivated at MO among the genera. The AF229769 T (MO) Vietnam AF229732 (MO) New Caledonia AF229731

(MO)(MO) New Caledoniahighest divergence Taiwan was between AF229728 Gastonia rodriguen- AF229768 (CHR 502422) Cult. in Halswell, New Zealand U63192 (CHR 485642) Cult. in Lincoln, New Zealand U63188 (CS) Mexico AF242231

(CS) Cult. in Botanical Gar den,sis Univ. Tokyo, J and Pentapanax racemosus; the lowest value was (CS) Cult. in South China Bot. Garden AF242247

(SYS)between Eleutherococcus Cult. South China Bot. Garden simonii and AF242244 Kalopanax pic- tus. In general, Gastonia was the most divergent of all taxa in Araliaceae, with distances ranging from J. Wen 2478 F. Chiang s.n. G.M. Plunkett 1378 G. Hao 901 A. Mitchell s.n. Acc# 18225 (CHR 500664)G.M. Plunkett 1359 LowryP.P. 4726 A. Mitchell s.n. P. P. Lowry 4920 S. Shi 11 Peel Forest Nursery, New Zealand LowryP.P. 4967 U63164 G.M. Plunkett 1315 P. P. Lowry 4648 10.143 to 20.724%. Phylogenetic Analyses. The parsimony analysis of the entire ITS region resulted in 14,580 maxi- mally parsimonious trees (MPTs) with a total length of 1,267 steps, a consistency index (CI) of 0.487 (0.416 excluding uninformative characters), and a retention index (RI) of 0.599. The strict con- sensus of the MPTs is presented in Fig. 1. A par- simony analysis in which the alignment gaps were coded as additional binary characters generated

Species over 10,000 MPTs with a total length of 1337 steps, A. Gray A. Gray J.D. Hook. & Thomson Griseb. Merrill ex Li (Hook.) K. Koch

Harms a CI of 0.487 (0.413 excluding uninformative char- (Hayata) Li Baillon

Hayata acters), and a RI of 0.594. Analyses in which gaps (Hook.) A.D. Mitchell, Baillon J. R. & J. G. Forst.

Vis. were treated either as missing data or as new char- acters generated very similar topologies, but the lat- ter helped to resolve the positions of both Fatsia (sister to the clade of Dendropanax-Hedera-Brassaiop- sis-Oreopanax-Gamblea and allies) and Tetrapanax D. Frodin & M. Heads Tetrapanax papyriferus Raukaua anomalus Trevesia palmata Reynoldsia sandwicensis Schefflera arboricola Schefflera candelabra Sciadodendron excelsum Schefflera minutistellata Sinopanax formosana Tupidanthus calyptratus Tetraplasandra hawaiiensis Schefflera digitata Schefflera gabriellae Schefflera hypoleucoides * * (sister to the clade of Heteropanax-Schefflera and 2001] WEN ET AL.: ARALIACEAE EVOLUTION 151

FIG. 1. The strict consenus tree of 14,580 maximally parsimonious trees (MPTs) of the core Araliaceae with the entire ITS sequences. The MPTs have 1267 steps, a CI of 0.487 (0.416 excluding uninformative characters), and a RI of 0.599. Taxa included in the broadly defined Schefflera are boldfaced. Numbers above lines are the decay indices and those below are bootstrap values in 1000 replicates, each with 100 trees. 152 SYSTEMATIC BOTANY [Volume 26 close allies). In addition, the placement of the Poly- Astrotricha and Osmoxylon form successive sister scias guilfoylei—P. fruticosa clade differs between the groups to all other species in core Araliaceae, but two analyses. This clade is sister to the clade com- the precise placement of these two genera at the prising Polyscias, Gastonia, Reynoldsia A. Gray and base of Araliaceae differs among the MP, NJ, and close allies when gaps were treated as missing data, ML trees (see Figs. 1–3). but in the tree in which gaps were treated as ad- ditional characters, the P.guilfoylei—P.fruticosa clade DISCUSSION is sister to a larger clade comprising not only Poly- scias, Gastonia, and Reynoldsia, but also Pseudopanax, Phylogenetic Relationships in Araliaceae. The Meryta and their close allies. Lastly, a weighted par- most widely used classification of Araliaceae is that simony analysis (weighting transversions over tran- of Harms (1898; see Table 1), who divided Arali- sitions 1.8 times based on actual estimates) for the aceae into three tribes (Schefflereae, Aralieae, and entire data set generated over 10,000 MPTs with a Mackinlayeae) mostly on the basis of petal mor- total length of 1267 steps, a CI of 0.487 and a RI of phology and aestivation. Our sample included 27 of 0.599. The topology of this analysis is very similar the 36 genera from Harms’ tribe Schefflereae. Of the to that in which gaps were treated as new charac- nine genera not sampled, eight have been trans- ters, differing only in the relative position of the P. ferred to larger genera [viz., Boerlagiodendron to Os- guilfoylei-P. fruticosa clade. moxylon (Philipson 1976; Lowry 1989); Crepinella to Trees resulting from the neighbor-joining analy- Schefflera (Frodin 1975; Maguire et al. 1984), Didy- sis (Fig. 2) and the maximum likelihood analysis mopanax Decne & Planchon to Schefflera (Maguire et (log likelihood of Ϫ7971.08; Fig. 3) were largely al. 1984; Frodin 1989); Eremopanax Baillon to Ar- congruent with the MPTs. There were, however, throphyllum (Philipson 1978a); Hederopsis to Macro- several notable differences, including the relative panax (Philipson 1979); Kissodendron, Nothopanax, positions of Osmoxylon and Astrotricha, and the po- and Sciadopanax to Polyscias (Bernardi 1971; Philip- sitions of Fatsia japonica, Oplopanax japonicus, Schef- son 1978b, 1979; Lowry 1989; see Table 1]. Apart flera candelabra, S. digitata, and Tetrapanax papyriferus from these, our sample lacked only Plerandra. In the (cf. Figs. 1–3). trees based on ITS data, Schefflereae appears to be All trees resulting from the analysis of ITS se- paraphyletic with regard to the four taxa sampled quences resolve two major clades, labeled the ’’A- from tribe Aralieae. ralia-Polyscias-Pseudopanax group,’’ and the ’’Eleu- Within tribe Aralieae, we sampled four of the 11 therococcus-Dendropanax-Schefflera group.’’ The Ara- genera included by Harms (1898): Aralia, Panax, lia-Polyscias-Pseudopanax group includes Aralia, Ar- Pentapanax, and Sciadodendron. It is clear, however, throphyllum Blume, Cuphocarpus Decne & Planchon, that Harms’ concept of tribe Aralieae was quite het- Gastonia, Meryta, Munroidendron Sherff, Panax, Pen- erogeneous, for all but two (Motherwellia and Harm- tapanax, Polyscias, Pseudopanax, Reynoldsia, Sciadod- siopanax Warb.) of the seven unsampled genera endron, and Tetraplasandra. The Eleutherococcus-Den- have now been excluded from core Araliaceae. For dropanax-Schefflera group includes Brassaiopsis Dec- example, recent molecular data suggest that the ne & Planchon, Dendropanax, Eleutherococcus, Fatsia, largely New Caledonian genera Delarbrea and My- Gamblea C. B. Clarke, Hedera, Heteropanax, Kalopanax, odocarpus (along with the New Caledonian endemic Macropanax, Metapanax, Oplopanax, Oreopanax, Schef- Pseudosciadium) form a clade within the order Api- flera, Sinopanax H. L. Li, Trevesia, and Tupidanthus. ales, but outside core Araliaceae (Plunkett et al. The Aralia-Polyscias-Pseudopanax group may be fur- 1996a, 1997, and unpublished). Stilbocarpa presents ther divided into two subclades: a mostly north a similar situation. This genus of three megaherb temperate Aralia-Panax clade and the more or less species is endemic to the subantarctic islands of tropical/subtropical Polyscias-Pseudopanax clade (al- New Zealand (Philipson 1965). Hooker (1853) orig- though many Pseudopanax have a south-temperate inally referred these species to Aralia, and Harms to subtropical distribution). Excluded from both (1898) placed Stilbocarpa in tribe Aralieae. A recent major clades, however, were a small number of study based on ITS sequences, however, suggests taxa, including Schefflera digitata, S. candelabra, Cus- that this genus is more closely related to Schizeilema sonia spicata, the Raukaua anomalus—Cheirodendron (Hook. f.) Domin. and Azorella Lam. of Apiaceae trigynum clade, and Cephalaralia cephalobotrys. Rela- (subfamily Hydrocotyloideae) than to any of the ar- tive to the major clades, these excluded species aliaceous genera (Mitchell et al. 1999). Lastly, Aral- form either a polytomy or a basal grade. In all trees, idium has been excluded from the order Apiales al- 2001] WEN ET AL.: ARALIACEAE EVOLUTION 153

FIG. 2. The neighbor-joining tree of the core Araliaceae based on Kimura two-parameter distances. 154 SYSTEMATIC BOTANY [Volume 26

FIG. 3. The maximum likelihood tree of the core Araliaceae constructed from the entire ITS sequences with a log likelihood of Ϫ7971.08. The numbers indicate branch length. 2001] WEN ET AL.: ARALIACEAE EVOLUTION 155 together. This monotypic genus from western Ma- ules extending into an appendage at the base of the lesia is now recognized as its own family, Aralidi- petiole; (3) panicles that have ultimate inflorescenc- aceae (Philipson and Stone 1980), or even its own es of umbels, capitula, racemules, or spicules; (4) order, Aralidiales (Takhtajan 1987). Recent studies the absence of pedicel articulations; (5) ovaries with based on rbcL data (Plunkett et al. 1996a; Xiang and 2–5 (or sometimes more) locules; and (6) no prickles Soltis 1998) suggest that Aralidium is allied to Tor- or arms on the vegetative organs (Frodin 1975, ricellia DC., Melanophylla Baker, and Griselinia For- 1986, 1989). Schefflera now includes ϳ650 species of ster & Forster f., which are the sister groups to the tropical and warm temperate trees, shrubs, lianas Apiales-Pittosporaceae clade. Apart from these ex- and epiphytes. Harms (1898) originally divided cluded taxa, all of the genera sampled from tribe Schefflera into two sections: sect. Cephaloschefflera Aralieae in the present study form a monophyletic Harms (species with sessile flowers) and sect. Eus- group (Figs. 1–3). chefflera (ϭ sect. Schefflera; species with pedicellate Lastly, tribe Mackinlayeae comprises just three flowers), but various other classifications of the ge- genera: Apiopetalum (2 spp. from New Caledonia), nus have also been proposed (e.g., Viguier 1909; Mackinlaya (5 spp. from east Malesia and the west- Hoo and Tseng 1965, 1978; Shang 1984). ern Pacific), and Pseudosciadium (1 sp. from New In addition to the six species listed as Schefflera Caledonia). All three, however, have been excluded in Table 2 (and Figs. 1–3), our sample also included from core Araliaceae on the basis of molecular data representatives of three additional genera often (Plunkett et al. 1996a, 1997, and unpublished). Be- placed under synonymy with Schefflera (viz., Bras- cause the focus of the present study is only the core saia, Dizygotheca, and Tupidanthus; see Lowry et al. group of Araliaceae, these excluded genera were 1989). Even on the basis of this limited sampling, not sampled herein; their placement within the or- ITS data suggest that Schefflera is polyphyletic. The der Apiales will be addressed in a subsequent position of the type species, Schefflera digitata, is not study. well resolved in the MPTs, but it forms one of five Emphasizing the inflorescence architecture and a clades in an unresolved polytomy toward the base few other characters including number of stamens, of the core Araliaceae clade (Fig. 1). In the NJ tree, petal aestivation and shape, and endosperm mor- Schefflera candelabra is placed in a subclade with phology, Hutchinson (1967) recognized seven tribes Cussonia, Raukaua,andCheirodendron, whereas Schef- in Araliaceae. This classification has been criticized flera gabriellae and Dizygotheca elegantissima form a by later Araliaceae workers such as Hoo and Tseng small clade with species of Mertya and Pseudopanax. (1978), Frodin (1982), Tseng and Hoo (1982), Wen Lastly, Schefflera arboricola, S. minutistellata, S. hypo- (1993), and Wen and Zimmer (1996) as being arti- leucoides, Brassaia actinophylla,andTupidanthus calyp- ficial, especially on the use of inflorescence struc- tratus form a subclade within the larger Eleuthero- ture as a delimiting character at the tribal level. coccus-Dendropanax-Schefflera clade. These results Hutchinson (1967) treated all taxa with racemose or confirm that segregate genera such as Tupidanthus spicate inflorescence in his tribe Cussonieae, which and Brassaia are closely related to various species consists of Agalma Miq. (ϭ Schefflera), Botryopanax presently assigned to Schefflera, but this broadly-de- Miq. (ϭ Polyscias), Cussonia, Gelibia Hutch. (ϭ Polys- fined genus appears to comprise no fewer than four cias), Munroidendron, and Parapentapanax Hutch. (ϭ different and well-separated evolutionary lineages Pentapanax). The ITS phylogeny clearly suggests in core Araliaceae, a result that is congruent with that taxa of tribe Cussonieae form a polyphyletic the polymorphic pollen morphology of this genus group (Figs. 1–3). (Tseng and Shoup 1978). The circumscription of Phylogeny and Taxonomic Status of Araliad Schefflera should be re-evaluated using a phyloge- Genera. THE POLYPHYL OF SCHEFFLERA. The larg- netic framework with both molecular and morpho- est genus in core Araliaceae is Schefflera, and recent logical characters. taxonomic treatments of the genus (Frodin 1975, THE PLACEMENT OF HETEROPANAX. The genus 1986, 1989; Maguire et al. 1984; Lowry et al. 1989) Heteropanax comprises approximately five species have placed several other genera (e.g., Brassaia from southern Asia and China, and is characterized Endl., Didymopanax, Dizygotheca, Sciadophyllum P. B r., by bicarpellate ovaries, divided styles, and leaves and Tupidanthus) under its synonymy. Typified by that are 2–5 times pinnately compound. The phy- S. digitata (from New Zealand; see Frodin 1975), logenetic position of this genus has, however, been Schefflera is presently defined as all araliads with controversial. Seemann (1868) placed it alongside (1) once palmately compound leaves; (2) fused stip- Brassaiopsis, Cussonia, Macropanax, Sciadopanax (ϭ 156 SYSTEMATIC BOTANY [Volume 26

Polyscias), and Sphaerodendron Seem. (ϭ Cussonia)in would have to be submerged within Polyscias to his tribe Cussonieae because these taxa all share render it monophyletic. bicarpellate ovaries, ruminate albumen, and an Within this very broad Polyscias clade, Reynoldsia, equal number of stamens and petals. Harms (1898) Munroidendron, Tetraplasandra, Gastonia, Polyscias ses- assigned Heteropanax to his broadly defined tribe silifolia, and Cuphocarpus form a well supported Schefflereae, regarding it as a close relative of Cus- subclade. Morphological and geographic evidence sonia and Schefflera. Hutchinson (1967), however, have been used to suggest a close relationship treated it in his tribe Hedereae along with the fol- among Gastonia, Munroidendron, Reynoldsia, and Te - lowing genera: Arthrophyllum, Boninofatsia Nakai (ϭ traplasandra, a subject discussed in depth by Philip- Fatsia), Brassaiopsis, Euaraliopsis Hutch., Gamblea, son (1970b), who also noted a close alliance of this Hedera, Hederopsis (ϭ Macropanax), Macropanax, Neo- complex to Polyscias. ITS data confirm a close rela- cussonia Hutch. (ϭ Schefflera), Oreopanax, and War- tionship among all these taxa, and a more detailed denia King (ϭ Brassaiopsis), on the basis of stamen treatment of this finding will be addressed in a sub- number (equal to petal number), petals characters sequent publication (G. M. Plunkett and P. P. Lowry, (unclawed, with valvate aestivation), inflorescence unpublished). structure (simple or compound umbels or heads, THE POSSIBLE RELATIONSHIP OF SINOPANAX TO OR- often paniculately or racemosely arranged), and ru- EOPANAX. A sister-group relationship between the mono- minate endosperm. Hoo and Tseng (1978) treated typic Sinopanax and the much larger genus Oreopan- Heteropanax in their tribe Tetraplasandreae along ax (ϳ80 species) is suggested by all three analyses with many other araliaceous genera with pinnately of ITS sequence data (MP, NJ, and ML; see Figs. 1– compound leaves (such as Polyscias). More recently, 3). Sinopanax formosana is endemic to Taiwan and Shang and Callen (1988) proposed a close relation- was originally described by Hayata (1908) as Or- ship of Heteropanax to Aralia and Panax. In the ITS eopanax formosana. Li (1949) segregated this species to establish a monotypic genus on the basis of its trees (Figs. 1–3), Heteropanax is sister to one of the capitate inflorescences. With Sinopanax formosana Schefflera subclades (viz., S. arborica, S. hypoleucoides, excluded, the remaining ϳ80 species of Oreopanax S. minutistellata, Brassaia actinophylla,andTupidan- are found only in Central and South America (al- thus calyptratus) within the Eleutherococcus-Hedera- though fossil evidence suggests that Oreopanax was Schefflera group, and is well separated from Polyscias also once distributed in North America; Dilcher and and the other genera of Hoo and Tseng’s tribe Te- Dolph 1970). Both genera share palmately-lobed traplasandreae (which are all placed in the Aralia- simple leaves, large terminal panicles of small cap- Polyscias-Pseudopanax clade in the ITS trees). The itate inflorescences, bilocular ovaries, and ruminate disparity between the morphological characters of endosperm. Additional data are needed to explore Heteropanax and those of the Schefflera subclade sug- the disjunct biogeographic relationship between the gests that additional work is needed to address re- Asiatic Sinopanax and the neotropical Oreopanax, lationships among these taxa. and to assess the taxonomic status of these two gen- THE PARAPHYLY OF POLYSCIAS. In Araliaceae, Po- era. lyscias is second only to Schefflera in number of spe- THE PROBLEM OF PANAX AND ITS RELATIONSHIP TO ϳ cies, with 130 species mostly from the paleotrop- ARALIA. The problem of circumscribing the genus ics. Polyscias was broadly defined by Philipson Panax has resulted in great confusion regarding its (1978b, 1979) as comprising those araliads with phylogenetic position within the family. First de- pinnately compound leaves and articulated pedi- scribed by Linnaeus (1735) in his Systema Naturae, cels. Treating the Malesian species, Philipson Panax initially included just two species, P.quinque- (1978b, 1979) divided the genus into five sections folius L. and P. trifolius (Linnaeus 1753); shortly based on morphology of stipules and inflorescenc- thereafter, P. fruticosus L. was added (Linnaeus es. The present study included ITS sequences from 1763). However, Linnaeus’ (1754) concept of Panax six species of Polyscias, but even with this limited (based mostly on floral morphology) was so broad- sampling, the ITS trees do not support a broad cir- ly defined that it would include most species cur- cumscription of this genus. Instead, Polyscias ap- rently placed in Araliaceae. Consequently, later pears to form a paraphyletic group within the Ara- workers (e.g., de Candolle 1830) referred many ad- lia-Polyscias-Pseudopanax clade. No fewer than six ditional species to this genus, leading Seemann other genera (viz., Arthrophyllum, Cuphocarpus, Gas- (1868: 52) to regard Panax as ‘‘one of the great lum- tonia, Munroidendron, Reynoldsia, and Tetraplasandra) ber-rooms of our science.’’ Seemann (1868) thus 2001] WEN ET AL.: ARALIACEAE EVOLUTION 157 narrowed the delimitation of Panax to include only 1978; Shang 1985a), a genus now submerged within the species closely related to P. quinquefolius and P. Polyscias (Lowry et al. 1989). Philipson (1965) in- trifolius. Harms (1897), discussing the morphology cluded these Chinese species of ’’Nothopanax’’ (i.e., and taxonomic history of Panax, followed Seemann’s Metapanax) within Pseudopanax, but Hoo and Tseng generic concept, and Britton and Brown (1913) des- (1978) suggested a close relationship to Merrillio- ignated Panax quinquefolius as the type species. panax H. L. Li. In our sample, we were able to sam- In several systems, such as those by Decaisne and ple both species of Metapanax and several species Planchon (1854), Bentham and Hooker (1867), and each of Pseudopanax and Polyscias, but unfortunately Clarke (1879), Panax (as typified by P. quinquefolius) no representatives of Merrilliopanax could be includ- has been submerged within Aralia. Confusingly, ed. Given this sampling limitation, the resulting ITS Bentham and Hooker (1867) placed the ginsengs trees suggest that the two species Metapanax are (e.g., Panax quinquefolius)inAralia, but recognized most closely related to Macropanax (Figs. 1–3), and a quite distinct genus ’’Panax’’ that included species not to either Pseudopanax or Polyscias. currently fitting the generic concept of Polyscias This result is well supported by morphological (with a woody habit and valvate aestivation). Ben- evidence. The two species of Metapanax are clearly tham and Hooker thus treated Aralia (with imbri- differentiated from both Pseudopanax and Nothopan- cate petals) and their ’’Panax’’ in different tribes. ax/Polyscias. Metapanax differs from Pseudopanax in Hutchinson (1967) also treated them in different inflorescence architecture and breeding systems tribes, but to add to the confusion, his ’’Panax’’ in- (Mitchell et al. 1997; Wen and Frodin, in press). The cluded both the herbaceous ginsengs (true Panax as species of Metapanax are hermaphrodite with ter- typified by P. quinquefolius) and the woody species minal umbels arranged racemosely, whereas the that are now placed in Polyscias (Philipson 1951). species of Pseudopanax are dioecious and have ter- Harms (1897) and Hoo (1961) regarded Panax as minal umbels arranged in umbellate clusters. The derivatives of an herbaceous Aralia. Hoo (1961) also two genera are also distinct geographically: Meta- suggested that Panax may have been derived from panax occurs in central and southwestern China Acanthopanax (ϭ Eleutherococcus). Wen (1993), Wen and Vietnam, whereas Pseudopanax is native to New and Zimmer (1996), Wen and Nowicke (1999) have Zealand, Tasmania, New Caledonia, and Chile. Al- argued on the basis of morphological, molecular, though the definition of Polyscias (including Notho- and pollen-ultrastructural data that the closest rel- panax) remains poorly-defined at present, Metapan- ative of Panax may be Aralia, a finding supported ax is easily distinguishable from most species of by the present ITS analysis (albeit weakly; decay Polyscias on the basis of leaf architecture (simple or value ϭ 1) (Figs. 1–3). Indeed, the only major dif- palmately compound in Metapanax, vs. pinnately ference between the two genera lies in their leaf compound in Polyscias, Stone 1965). Lastly, the re- architecture (palmately compound in Panax vs. bi- lationship between Metapanax and Macropanax sug- or tripinnately compound in Aralia) and carpel gested by the ITS trees is supported by the shared number (2–3 in Panax vs. 5–8 in Aralia), but Wen presence of evergreen leaves, mostly dentate leaflet (1993) regarded these characters as evolutionarily margin, paniculately arranged umbel inflorescence, labile in Araliaceae (e.g., 4–5-locular ovaries are not hermaphrodite flowers, and a 5-carpellate ovary. uncommon in Panax as developmental abnormali- The two genera can, however, be distinguished by ties; J. Wen, pers. obs.). In contrast, Panax and Aralia their different endosperm types (uniform in Meta- share many features, including imbricate floral aes- panax, ruminate in Macropanax), the division of tivation, uniform endosperm, and similar pollen styles (divided in Metapanax, undivided in Macro- morphology and ultrastructure. Eyde and Tseng’s panax), and fruit shape (somewhat flattened in Me- (1971) study of floral vasculature and the combined tapanax, globose to subglobose in Macropanax) rbcL–matK study of Plunkett et al. (1997) provide (Shang 1985b). further evidence of a close relationship between THE BRASSAIOPSIS—EUARALIOPSIS—TREVESIA SUBCLA- these two genera. DE. Species now placed in Euaraliopsis were orig- THE RELATIONSHIP BETWEEN MACROPANAX AND inally included in Brassaiopsis Decne & Planchon. METAPANAX. Metapanax is a newly-established ge- Hutchinson (1967), however, established Euaraliop- nusoftwospecies(M. davidii and M. delavayi) from sis to accommodate those taxa with simple, lobed China and Vietnam (Frodin 1992; Wen and Frodin, leaves; the remaining species of Brassaiopsis all have in press). The Chinese species of Metapanax were palmately-compound leaves. The two genera do, previously included in Nothopanax (Hoo and Tseng however, share many characteristics, including un- 158 SYSTEMATIC BOTANY [Volume 26 jointed pedicels, bilocular ovaries, undivided stig- (Stace 1993). The relatively high level of infraspe- mas, and ruminate endosperm. Hoo and Tseng cific variation (in terms of both morphology and the (1978) accepted the generic status of Euaraliopsis, ITS sequences) suggests the need for a careful tax- but other workers (e.g., Philipson 1979; Shang onomic evaluation of the species. 1985c; Hoˆ1993) treated it under the synonymy of ELEUTHEROCOCCUS AND PUTATIVE RELATIVES. Brassaiopsis. Hoo and Tseng (1978) suggested that Eleutherococcus (often known under its synonym Euaraliopsis may be closely related to Trevesia be- Acanthopanax) is a relatively large and diverse ge- cause the leaf lobes of both genera sometimes have nus with 31 species endemic to Asia (Ohashi 1987a; pseudopetiolules (see Hoo and Tseng 1978, pl. 1, f. Kim 1997), and delimitation of this genus remains 7), and that Brassaiopsis was perhaps related to or a controversial. Morphologically, Eleutherococcus in- derivative of Schefflera. Tseng and Hoo (1982) sug- cludes shrubs with 5-merous flowers, 2–5 carpels, gested that Trevesia, with its 5-locular ovary, was and prickles on the leaves, petioles, or twigs. Harms more ‘‘primitive’’ than Euaraliopsis. Philipson (1979) (1918) also included Kalopanax within Acanthopanax argued that dividing Brassaiopsis into two genera: (i.e., Eleutherococcus), but later workers (e.g., Hoo Brassaiopsis s. str. and Euaraliopsis fragmented a co- and Tseng 1978; Lee 1993; Ohwi 1984; Shang 1985a; herent assemblage. Philipson (1979) also suggested Ohashi 1994) have generally recognized Kalopanax a possible close relationship between Brassaiopsis s.l. as distinct. Mitchell and Wagstaff’s (1997) study of and Trevesia based on their similar vegetative char- morphology and ITS data confirmed Harms’ earlier acters. Brassaiopsis s.l. and Trevesia can, however, be treatment, and this finding is supported by the pre- distinguished by Trevesia‘s more massive inflores- sent (broader) analysis ITS data from throughout cences and its ovaries with more locules (5 vs. 2). Araliaceae. Moreover, sister to this Eleutherococcus— The ITS trees confirm a close relationship among Kalopanax group is the clade comprising Macropanax these three or two genera, suggesting that Brassaiop- and Metapanax. These four genera are similar in sis, Euaraliopsis, and Trevesia form a well supported both inflorescence structure and floral morphology, clade (decay index ϭ 5). The generic status and de- but the two subclades may also be clearly differ- limitation of Brassaiopsis, Euaralipsis, and Trevesia, entiated: Eleutherococcus and Kalopanax are decidu- however, need to be carefully examined. ous and generally have prickles on the stem, where- THE PLACEMENT OF HEDERA. The genus Hedera, as Macropanax and Metapanax are evergreen and un- and in particular H. helix (English ivy), is well- armed. known for its horticultural importance. It comprises Another potential ally of Eleutherococcus is the ge- 8–12 species from Eurasia, but its taxonomy is high- nus Gamblea (3 species), which is now thought to ly problematic. The species of Hedera are evergreen include Evodiopanax as well (e.g., Mabberley 1997); climbers with heteroblastic foliage in which the ju- nomenclatural transfers to Gamblea, however, have venile and adult leaves vary within individuals in not yet been formally made. Gamblea was first de- terms of leaf shape, size, and lobing. They have pa- scribed by Clarke (1879) on the basis of the Hima- niculate umbels, unjointed pedicels, polygamous layan species G. ciliata C. B. Clarke. Evodiopanax, of- flowers, valvate aestivation, 5-locular ovaries, and ten treated under synonymy with Eleutherococcus ruminate endosperm. Previous workers (e.g., (e.g., Harms 1898, 1918; Hoo and Tseng 1978; Ohwi Harms 1898; Hoo 1961; Shang and Callen 1988) 1984), was originally defined by Nakai (1924) based have generally regarded Hedera as a closely related on material from Japan. Although Kim (1997) re- to or derived from Dendropanax, and this close re- cently retainted the generic status of Evodiopanax lationship is supported by the NJ tree of the ITS (including within it four species from eastern to phylogeny (Fig. 2). The MP and ML trees do sug- southeastern Asia), these species share with Gam- gest that Hedera is closely related to Dendropanax, blea many features, including the presence of long but it may be closer to the Brassaiopsis—Euaraliop- and short shoots, polygamo-dioecious flowers, a 4– sis—Trevesia clade (cf. Figs. 1, 3). The phylogenetic 2-locular ovary, and the lack of prickles. The erec- position of Hedera needs to be explored with addi- tion of two distinct genera to accommodate such a tional datasets. homogeneous group of species is likely due to re- Our sampling included two accessions of Hedera gional treatments lacking a more broadly-based helix, both from cultivation. Pairwise comparison of geographical perspective. In the present study, two the ITS sequences from these two accessions was species from this group were sampled, Gamblea 1.0%. Morphologically, Hedera helix is a highly var- pseudoevodiaefolia and Evodiopanax innovans. The ITS iable species, especially with regard to leaf shape trees (cf. Figs. 1–3) confirm the close relationship of 2001] WEN ET AL.: ARALIACEAE EVOLUTION 159

Gamblea and Eviodiopanax, but suggest that these Aralia, Arthrophyllum, Cephalaralia, Gastonia, Hetero- taxa are not closely allied to Eleutherococcus and its panax, Munroidendron, Pentapanax, Polyscias, and Rey- relatives. noldsia. Simple leaves are often regarded as unusual Character Evolution. The taxonomy of Arali- in Araliaceae, but in fact they are found among sev- aceae has relied heavily on just a few morphological eral genera (e.g., Astrotricha, Dendropanax, Fatsia, characters, notably petal aestivation, inflorescence Hedera, Hunaniopanax C. J. Qi & T. R. Cao, Meryta, architecture, leaf architecture, and carpel number. Oplopanax, Oreopanax, Sinopanax, and Tetrapanax). The evolution of these characters has been dis- Moreover, ancestral character analysis of the ITS cussed by Philipson (1970a), Eyde and Tseng trees suggests that simple leaves are ancestral in (1971), Frodin (1982), and Plunkett et al. (1996a, core Araliaceae, despite the traditional notion that 1997), but these studies have lacked either the phy- Araliaceae ‘‘terminate a long-line of compound- logenetic framework or the broad sampling avail- leaved’’ plants (Cronquist 1981). This result is con- able in the present study. Therefore, we review and sistent with the findings of Plunkett et al. (1996a, re-evaluate the evolution of these taxonomically im- 1997), who suggested that simple leaves were ple- portant characters in light of the ITS phylogenies. siomorphic throughout the entire order Apiales. In doing so, we have applied the principles and It must be noted, however, that many araliads concepts of ancestral area analysis (Bremer 1992) to also have heteroblastic leaves. In these species, the determine plesiomorphic character states using the leaf morphology changes in a single individual topology from the parsimony analysis (Fig. 1). with developmental stage and/or habitat (e.g., from PETAL AESTIVATION. All genera of Araliaceae palmately or pinnately lobed/compound to simple, have valvate aestivation except those traditionally or vice versa). Well-known examples of heteroblas- referred to tribe Aralieae (Table 1). The present tic leaves are those found in Hedera, Trevesia, and study included samples from five of these imbricate Cussonia. We coded simple leaves as a single char- genera: Aralia, Cephalaralia, Panax, Pentapanax, and acter state in the present study, but future studies Sciadodendron. The ITS trees suggest that valvate (with a broader sampling) might address the po- petals were plesiomorphic in core Araliaceae and larity of this character state within each heteroblas- that imbricate petals evolved independently at least tic genus. Further, it cannot be assumed that all two times: once in Cephalaralia and a second time simple leaves in Araliaceae are homologous. Astro- in the clade comprising Aralia, Panax, Pentapanax, tricha and Dendropanax, for example, have simple and Sciadodendron. Several taxa now excluded from and undivided leaves with pinnate venation, but core Araliaceae (and not sampled in the present the leaves of Oreopanax, Oplopanax, and Tetrapanax study) also have imbricate aestivation, and thus are simple and palmately divided, and those of likely represent additional independent origins of Trevesia are simple but variously divided. Lastly, the imbrication. For example, the imbricate Stilbocarpa simple leaves of some species or genera appear to (traditionally placed in tribe Aralieae; Harms 1898) be secondarily derived from compound leaves, such is highly divergent from all other araliaceous gen- as the unifoliolate leaves in some species of Poly- era, and the study of ITS sequences by Mitchell et scias, or the ‘‘simple’’ leaves of Meryta and Hunan- al. (1999) confirms that this genus should be ex- iopanax (which maintain petiolule articulations cluded from core Araliaceae. The closely related along the midrib). ‘‘Simple’’ leaves in Hunaniopanax family Apiaceae is also largely characterized by val- may be evolved from the pinnately compound vate aestivation, but there are some imbricate mem- leaves of its close relatives such as Pentapanax (Qi bers of that family as well. Members of Pittospor- 1988). Thus, additional studies of these genera are aceae, on the other hand, have petals that are either needed to more thoroughly assess the polarity and united or imbricate. homologies of leaf architecture in core Araliaceae. LEAF ARCHITECTURE. Leaf type in Araliaceae is CARPEL NUMBER. Most genera in Araliaceae extremely diverse, varying from simple and entire, have inferior ovaries with 2–5 carpels (represented to simple and variously lobed, to compound (either by 2–5 locules), each with a single functional ovule palmately, ternately, or once-, twice-, or thrice-pin- (Philipson 1970a). A few genera (e.g., Gastonia, Pler- nately compound). Palmately compound leaves are andra, and Reynoldsia), however, have as many as 20 quite common, as examplified by Cheirodendron, carpels, and the locule number of the anomalous Eleutherococcus, Gamblea, Macropanax, Panax, Schef- Tupidanthus calyptratus can be as great as 200. The flera, and most species of Pseudopanax. Pinnately polarity of locule number in Araliaceae has re- compound leaves characterize all or most species of ceived much attention. Most workers (e.g., Harms 160 SYSTEMATIC BOTANY [Volume 26 2001] WEN ET AL.: ARALIACEAE EVOLUTION 161

1898; Li 1942; Baumann-Bodenheim 1955; Philipson section Aralia and the single species of section Na- 1970a; Eyde and Tseng 1971) regarded the pluri- nae Harms (Aralia nudicaulis). In the present study, carpellate ovary as primitive in Araliaceae, a find- we sampled two herbaceous species from section ing that both Philipson (1970a) and Eyde and Tseng Aralia (A. apioides and A. racemosa); these form a (1971) believed was well supported by patterns of monophyletic group. The placement of section Ara- floral vasculature. In contrast, some workers have lia relative to the herbaceous species in Panax is un- suggested that pentacarpellate (Cronquist 1968, but resolved in the MP trees (Fig. 1), but the NJ and see also Cronquist 1981) or bicarpellate (Plunkett et ML trees (Figs. 2, 3) indicate that they are not sister al. 1996a, 1997) ovaries were ancestral not only in groups. This suggests that the herbaceous habit Araliaceae but throughout Apiales. Determining may have evolved independently in Aralia and Pan- the precise placement of Astrotricha and Osmoxylon ax. As discussed above, Stilbocarpa (not surveyed in at the base of core Araliaceae will have an impor- the present study) has been excluded from core Ar- tant impact on the interpretation of this character aliaceae on the basis of molecular data (Mitchell et in Araliaceae. The MP trees suggest a basally- al. 1999). Thus, the origin of herbaceousness in this branching position for Astrotricha, a genus of 15–20 genus can be regarded as independent of that in species all having bicarpelate ovaries (see Bean Aralia and Panax. 1991). This topology would be consistent with the Biogeography. A striking feature of the ITS theory of Plunkett et al. (1996a, 1997). If, however, trees (Figs. 1–3) is the relatively short branch Osmoxylon occupies this position (as the NJ tree lengths characterizing all the deeper nodes of the suggests), the interpretation of carpel-number po- trees. Among the possible explanations is that core larity becomes much more difficult. Carpel number Araliaceae may have experienced a rapid diversi- in the ϳ50 species of Osmoxylon ranges from 1–25 fication early in its evolutionary history. In both of or more (Philipson 1979), and thus the plesiom- the major clades within the family (the Eleuthero- orphic condition within this genus would need to coccus—Dendropanax—Schefflera group and the Ara- be established before carpel-number polarity could lia—Polyscias—Pseudopanax group), there are both be determined for the family. The ambiguity of temperate and tropical subclades (Fig. 4). The pre- these results highlights the limitations of a study sent-day distribution of Araliaceae, however, is best that uses a small number of exemplar species to developed in the tropics and subtropics (particu- represent a much larger group of plants. This lim- larly in southeastern/southern Asia and the Pacific itation notwithstanding, it is clear that pluricarpel- islands) and all of the basally-branching lineages in late ovaries have evolved from paucicarpellate ova- the family (e.g., Astrotricha, Cephalaralia, and ries at least two times in Araliaceae, once in Tupi- Osmoxylon) are endemic to the paleotropics. Cou- danthus, and another in Tetraplasandra and related pled with the present-day distributions of Pitto- genera. sporaceae and the basal lineages of Apiaceae (e.g., WOODY VS.HERBACEOUS HABIT. Araliaceae the mostly tropical and southern-hemisphere mem- comprise mostly woody taxa (trees, shrubs, or bers of subfamily Hydrocotyloideae, and the south- woody vines), with only a very few herbs. Al- ern-African, woody species of subfamily Apioi- though the closely-related family Apiaceae is most- deae; see Plunkett et al. 1996b; Downie et al. 1998), ly herbaceous, the basally-branching lineages of Araliaceae appear to have originated in the paleo- core Araliaceae (Astrotricha and Osmoxylon) and the tropics. species of the other close allies of Apiales (e.g., Pit- Despite their tropical origins, there are many ex- tosporaceae) are all woody. This confirms the tra- amples of north temperate taxa in the family, in- ditional notion that the woody habit is ancestral in cluding some or all members of Aralia, Eleutherococ- Araliaceae. The herbaceous species of the family are cus, Gamblea, Hedera, Kalopanax, Oplopanax, Panax, limited to just three genera, Aralia, Panax, and Stil- and Tetrapanax. The ITS topology suggests that the bocarpa. Within Aralia (55 spp., Wen 1993), 10 spe- origin of north temperate groups in Araliaceae is cies are herbaceous, including the nine species of quite complex. Broadly speaking, it would appear

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FIG. 4. The strict consensus tree of 10,000 maximally parsimonious trees as in Fig. 1, showing the biogeographic relationships among the tropical/subtropical and temperate taxa. Arrows indicate the evolution of temperate clades from subtropical/tropical ones. 162 SYSTEMATIC BOTANY [Volume 26 that the Aralia—Polyscias—Pseudopanax group arose in the tropical or subtropical regions, where many ACKNOWLEDGEMENTS. The authors thank Kyong-Jia members may still be found (e.g., Arthrophyllum, Lee, M. D. McBroom, and Suhua Shi for laboratory assis- Gastonia, Meryta, Munroidendron, Reynoldsia, and Te - tance; Fernando Chiang, Gang Hao, Pete Lowry, and Su- traplasandra). The largely north temperate Aralia— hua Shi for providing leaf material; Stephen Downie, Pete Lowry, an anonymous reviewer, and associate editor Alan Panax subgroup, therefore, most likely had a trop- Whittemore for valuable comments and suggestions; the ical origin. Conversely, in the Eleutherococcus—Den- National Science Foundation (DEB9726830) and the Na- dropanax—Schefflera group it appears that temperate tional Geographic Society for financial support to JW; and taxa may have arisen independently at least four the staff of ORSTOM Noume´a, CSIRO (Atherton and Can- times in the following clades (Fig. 4): the Eleuther- berra), and the National Geographic Society (5793–96) for ococcus—Kalopanax clade, the Evodiopanax—Gam- assistance to GMP. blea—Oplopanax clade, the Hedera clade, and the Te - trapanax clade. LITERATURE CITED In general, the ITS trees suggest that temperate taxa of Araliaceae are mostly derived from sub- ALLAN, H. H. 1961. Flora of New Zealand, vol. 1. Wellington: tropical and tropical members. On a narrower scale, Government Printer. some subtropical/tropical taxa are nested within BALDWIN, B. G., M. J. SANDERSON,J.M.PORTER,M.F. WOJCHIECHOWSKI,C.S.CAMPBELL, and M. J. DONO- the temperate ones. 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