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

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The Evolution of Araliaceae: a Phylogenetic Analysis Based on ITS Sequences of Nuclear Ribosomal DNA View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Lincoln University Research Archive Systematic Botany (2001), 26(1): pp. 144±167 q 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 Schef¯erieae (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-Schef¯era group'' (including Brassaiopsis, Dendropanax, Eleutherococcus, Fatsia, Hedera, Oreopanax, Schef¯era, 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 (Schef¯era, Pseudopanax) or paraphyletic (Aralia, Polyscias), but further studies will be needed to fully re-de®ne these complex taxa. Outgroup comparisons and the placement of Astrotricha and Osmoxylon (in basally-branching lineages in Araliaceae) help to con®rm 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 SinopanaxÐOreopanax 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 Paci®c 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 classi®cation 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), Schef¯era 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 de®ned Asteridae (Chase et al. 1993; later workers as ``arti®cial'' due to its heavy reliance Olmstead et al. 1993; Plunkett et al. 1996a; Soltis et on in¯orescence 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, in¯orescence struc- Araliaceae are characterized by relatively con- ture may be variable within a single genus (e.g., served ¯oral, but diverse vegetative features (Phi- Aralia, Wen 1991, 1993; Schef¯era, Frodin 1982) or lipson 1970a; Eyde and Tseng 1971). Members of even within a single section (e.g., Aralia sect. Aralia, the family possess ®ve 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 ®ve 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 re®nement 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' Schef¯ereae 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 classi®cation 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 ®ve ``series'' (5 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; Hoà uniform). Seemann (1868) de®ned the segregate 1993)]. Further, revisionary treatments have been ``order'' (5 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 ®ve tribes (Cussonieae, 1997), Macropanax (Shang 1983), and Schef¯era (Fro- Hors®eldieae, 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 5 12 is highly con- 1985a; Mabberly 1997), divides Araliaceae into served throughout the family, with diploid num- three tribes (Aralieae, Mackinlayeae, and Schef¯er- bers mostly of 2n 5 24 or 2n 5 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; LoÈve and Ritchie Schef¯ereae (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; LoÈve and LoÈve 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 5 192 (Stace 1993; Vargas 146 SYSTEMATIC BOTANY [Volume 26 TABLE 1. The classi®cation of Araliaceae according to Harms (1898). Modern synonymies are noted
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