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The Phylogeny and a New Classification of the Gingers (Zingiberaceae): Evidence from Molecular Data1

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The Phylogeny and a New Classification of the Gingers (Zingiberaceae): Evidence from Molecular Data1 American Journal of Botany 89(11): 1682±1696. 2002. THE PHYLOGENY AND A NEW CLASSIFICATION OF THE GINGERS (ZINGIBERACEAE): EVIDENCE FROM MOLECULAR DATA1 W. J OHN KRESS,2,5 LINDA M. PRINCE,2,4 AND KYLE J. WILLIAMS3 2Botany, MRC-166, United States National Herbarium, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, Washington, D.C. 20013-7012 USA; 3Department of Biology, Duke University, Durham, North Carolina 27708 USA The pantropical Zingiberaceae is the largest family in the order Zingiberales with 53 genera and over 1200 species. Classi®cations of the family ®rst proposed in 1889 and re®ned by others since that time recognize four tribes (Globbeae, Hedychieae, Alpinieae, and Zingibereae) based on morphological features, such as number of locules and placentation in the ovary, development of staminodia, modi®cations of the fertile anther, and rhizome-shoot-leaf orientation. New phylogenetic analyses based on DNA sequences of the nuclear internal transcribed spacer (ITS) and plastid matK regions suggest that at least some of these morphological traits are homo- plasious and three of the tribes are paraphyletic. The African genus Siphonochilus and Bornean genus Tamijia are basal clades. The former Alpinieae and Hedychieae for the most part are monophyletic taxa with the Globbeae and Zingibereae included within the latter. The results of these phylogenetic investigations are used to propose a new classi®cation of the Zingiberaceae that recognizes four subfamilies and four tribes: Siphonochiloideae (Siphonochileae), Tamijioideae (Tamijieae), Alpinioideae (Alpinieae, Riedelieae), and Zingiberoideae (Zingibereae, Globbeae). Morphological features congruent with this classi®cation and the taxonomic status of various monotypic genera are discussed. Key words: classi®cation; gingers; ITS; matK; phylogeny; tropical; Zingiberaceae; Zingiberales. The primarily tropical Zingiberales are phylogenetically em- Nagamasu, 2000; Kress and Larsen, 2001; Larsen and Jenjit- bedded within the derived eumonocots (Arecales, Commelin- tikul, 2001) newly described in the last several years. ales, Poales) and include many conspicuous taxa, such as the The currently accepted classi®cation of the Zingiberaceae bananas (Musaceae), birds of paradise (Strelitziaceae), heli- (Petersen, 1889; Schumann, 1904; Holttum, 1950; Burtt and conias (Heliconiaceae), and gingers (Zingiberaceae). With 53 Smith, 1972; Larsen et al., 1998) includes four tribes (Hedy- genera and over 1200 species, the Zingiberaceae is the largest chieae: 22 genera, Figs. 2±3; Alpinieae: 25 genera, Fig. 4; of the eight families of the order (Kress, 1990). In earlier clas- Zingibereae: one genus, Fig. 5; and Globbeae: four genera, si®cations (e.g., Petersen, 1889; Schumann, 1904) the family Fig. 6) and is based on both vegetative and ¯oral character- Costaceae (Fig. 1) was included in the Zingiberaceae, but with istics (Table 1). Although a number of morphological features a number of distinctive characters (e.g., lack of aromatic oils, have been used to distinguish the four tribes, in most cases branched aerial stems, and spiral monostichous phyllotaxy; the de®ning characters are either not unique to any one tribe Specht et al., 2001) it is now accepted as the sister clade to or are not universal for all taxa within any tribe (Table 1). For the gingers (Kress, 1990, 1995; Kress et al., 2001). The Zin- example, the plane of distichy of the leaves is perpendicular giberaceae is distributed pantropically with one genus (Re- to the rhizome in the Alpinieae (except in the genera Rhyn- nealmia) found in the Neotropics, four genera (Aframomum, chanthus and Pommereschea) and is parallel to the rhizome in Aulotandra, Siphonochilus, and Renealmia) found in Africa, the other three tribes (except for Siliquamomum in the Hedy- and the rest of the genera distributed in east Asia and the chieae). Similarly, the ovary is unilocular in all members of Paci®c Islands. The family is still poorly known taxonomically the Globbeae, but trilocular in the other three tribes with some with many species (Theilade and Mood, 1997; Sakai and Na- exceptions, e.g., unilocular in Tamijia and partially unilocular gamasu, 1998; Poulsen, Mood, and Ibrahim, 1999; Williams, in Caulokaempferia, Paracautleya, Scaphochlamys, Siphono- Kress, and Thet Tun, 2002) and even genera (Newman, 1995; chilus, and Riedelia (Larsen et al., 1998; Sakai and Nagamasu, Mood and Larsen, 1997; Larsen and Mood, 1998; Sakai and 2000). The lateral staminodes are well developed in Hedy- chieae, Globbeae, and Zingibereae (Figs. 2±3, 5±7) and gen- 1 Manuscript received 15 February 2002; revision accepted 3 May 2002. The authors thank Ray Baker, Josef Bogner, Mike Bordelon, Alan Carle, erally absent in the Alpinieae (Fig. 4; but all ®ve staminodes Mark Collins, David Harris, Yin Yin Kyi, Kai Larsen, Qing-Jun Li, Jing-Ping are absent in Rhynchanthus). The fusion of the lateral stami- Liao, Ida Lopez, Paul Manos, John Mood, Mark Newman, Chatchai Ngam- nodes to the central labellum (Fig. 7) in Siphonochilus (He- riabsakul, Dan Nicolson, David Orr, Louise Pedersen, Kai Rangsiruji, Shoko dychieae; Fig. 2) and Zingiber (Zingibereae; Fig. 5) has now Sakai, Henk van der Werf, Tom Wood, Qi-Gen Wu, and Yong-Mei Xia for been reported in the narrow endemic Tamijia (Alpinieae) from discussion, assistance, and tissue samples that made this investigation possi- ble. The comments of two anonymous reviewers signi®cantly improved the Borneo (Sakai and Nagamasu, 2000). Most of the characters manuscript. This work was funded by the Smithsonian Scholarly Studies Pro- that are used to de®ne the tribes are often inconsistent and gram, the Biotic Surveys and Inventories Program of the National Museum variable. of Natural History, and the A.W. Mellon Training Grant for Plant Systematics The circumscription of various genera of the Zingiberaceae to Duke University. has also been debated by investigators (e.g., Etlingera: Burtt 4 Current address: Rancho Santa Ana Botanic Garden, 1500 North College Avenue, Claremont, California 91711-3157 USA. and Smith, 1986; Curcumorpha: Larsen, 1997; Paramomum: 5 Author for reprint requests (phone: 202-357-2534; FAX: 202-786-2563; Wu, 1997), and a consensus has not been reached on the actual e-mail: [email protected]). number of genera in the family. Nearly one-quarter of the gen- 1682 October 2002] KRESS ET AL.ÐPHYLOGENY OF THE GINGERS 1683 Figs. 1±6. Representatives of the major groups of the family Zingiberaceae and the sister family Costaceae. 1. Costaceae (Monocostus). 2. Hedychieae (Siphonochilus). 3. Hedychieae (Hedychium). 4. Alpinieae (Alpinia). 5. Zingibereae (Zingiber). 6. Globbeae (Mantisia). era in the Zingiberaceae are monospeci®c, but no criteria for molecular analyses, to evaluate the status of monotypic genera the recognition of these species at the generic level have been where possible, and to construct a new phylogenetic classi®- established. One important question in the classi®cation of the cation of the family. family is how to determine the taxonomic status of these often morphologically very distinctive monospeci®c genera. MATERIALS AND METHODS Recently several papers have used molecular data to explore the phylogenetic relationships within the family Zingiberaceae TaxaÐWe sampled 104 species in 41 genera representing all four tribes of (Searle and Hedderson, 2000; Wood, Whitten, and Williams, the Zingiberaceae (http://ajbsupp.botany.org/v89/). In the larger genera (e.g., 2000) as well as within several genera (Hedychium: Wood, Alpinia, Curcuma, Hedychium, Globba, Zingiber) several species representing Whitten, and Williams, 2000; Alpinia: Rangsiruji, Newman, infrageneric morphological diversity were included. Unfortunately, for several important genera (e.g., Elettaria, Geocharis, Geostachys) we either did not and Cronk, 2000a, b; Roscoea: Ngamriabsakul, Newman, and have adequate tissue samples or we were not able to amplify DNA. We also Cronk, 2000; Aframomum: Harris et al., 2000). These analyses lacked adequate samples of a number of rare monospeci®c genera (e.g., Lep- have succeeded in clarifying the patterns of evolutionary re- tosolena, Parakaempferia, Paracautleya, Nanochilus, and Cyphostigma). lationships to varying degrees, but in general have been lim- ited in breadth of taxon sampling as well as resolution. OutgroupÐWe initially used representative taxa of the seven other families Our goal in the present study is to use molecular sequence of the Zingiberales as outgroups in our molecular analyses (http://ajbsupp. data to generate hypotheses on the phylogenetic relationships botany.org/v89/). However, because of the dif®culty of aligning the sequences among the genera of the Zingiberaceae in order to evaluate of the internal transcribed spacer (ITS) loci and matK-trnK ¯anking intergenic past classi®cations of the family, to identify morphological spacer regions in these other families with our ingroup taxa, we ®rst conducted features that characterize the various clades detected by the more focused analyses of the coding region of matK, which is easier to align 1684 TABLE 1. Characteristics and genera of the previously recognized tribes of the Zingiberaceae (after Schumann, 1904; Holttum, 1950; Burtt and Smith, 1972; Larsen et al., 1998). Authorities follow Reveal (2002). Tribes Character Alpinieae A. Rich. (1841) Hedychieae Horan. (1862) Globbeae Meisn. (1842) Zingibereae Meisn. (1842) 1) Plane of distichy of leaves perpendicular to rhizome parallel to rhizome parallel to
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