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The Molecular Phylogeny of Alpinia (Zingiberaceae): a Complex and Polyphyletic Genus of Gingers1

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The Molecular Phylogeny of Alpinia (Zingiberaceae): a Complex and Polyphyletic Genus of Gingers1 American Journal of Botany 92(1): 167±178. 2005. THE MOLECULAR PHYLOGENY OF ALPINIA (ZINGIBERACEAE): A COMPLEX AND POLYPHYLETIC GENUS OF GINGERS1 W. J OHN KRESS,2,3,5 AI-ZHONG LIU,2 MARK NEWMAN,4 AND QING-JUN LI3 2Department of Botany, MRC-166, United States National Herbarium, National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, D.C. 20013-7012 USA; 3Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan 666303 China; and 4Royal Botanic Garden, 20A Inverleith Row, Edinburgh EH3 5LR, Scotland, UK Alpinia is the largest, most widespread, and most taxonomically complex genus in the Zingiberaceae with 230 species occurring throughout tropical and subtropical Asia. Species of Alpinia often predominate in the understory of forests, while others are important ornamentals and medicinals. Investigations of the evolutionary relationships of a subset of species of Alpinia using DNA sequence- based methods speci®cally test the monophyly of the genus and the validity of the previous classi®cations. Seventy-two species of Alpinia, 27 non-Alpinia species in the subfamily Alpinioideae, eight species in the subfamily Zingiberoideae, one species in the subfamily Tamijioideae, and three species in the outgroup genus Siphonochilus (Siphonochiloideae) were sequenced for the plastid matK region and the nuclear internal transcribed spacer (ITS) loci. Parsimony analyses of both individual and combined data sets identi®ed six polyphyletic clades containing species of Alpinia distributed across the tribe Alpinieae. These results were supported by a Bayesian analysis of the combined data set. Except in a few speci®c cases, these monophyletic groupings of species do not correspond with either Schumann's (1904) or Smith's (1990) classi®cation of the genus. Here we build on previous molecular analyses of the Alpinioideae and propose the next steps necessary to recognize new generic boundaries in the Alpinieae. Key words: Alpinia; ¯existyly; gingers; ITS; matK; phylogeny; tropical; Zingiberaceae. Alpinia Roxb. is the largest and most widespread genus in & S.J. Chen and A. blepharocalyx K. Schum.) the plants form the Zingiberaceae with some 230 species occurring from Sri large stands in the understory, along forest margins, and in Lanka and the Western Ghats of India to China, Japan, all of light gaps, while other species are dominant in wetlands and southeast Asia, the Paci®c as far as Fiji, Samoa, and the Car- along water courses [e.g., A. nigra (Gaertn.) B.L. Burtt]. Al- oline Islands, and Australia as far south as northern New South though most alpinias are pollinated by large bees, some spe- Wales (Larsen et al., 1998; Smith, 1990). Most species grow cies attract birds and even bats as pollinators (Zhang et al., in low- to mid-elevation forests and form clumps with stems 2003; Kress and Specht, in press). Flexistyly, a novel ¯oral from 1±3 m high, although species east of Wallace's Line tend mechanism promoting outcrossing in which styles move up or to grow much larger. Alpinia regia R.M. Sm. of the Moluccas down depending on the timing of anther dehiscence, has been and A. boia Seem. of Fiji, for example, reach over 8 m in described in a number of species of Alpinia (Li et al., 2001, height. Some species are found in montane forests up to 2000 2002; Zhang et al., 2003). m above sea level in New Guinea and Sulawesi. However, The generic name Alpinia was ®rst used by Linnaeus for very few are tolerant of frost. The most northerly species is Alpinia racemosa, a neotropical species. Many Asiatic species Alpinia japonica (Thunb.) Miq., which survives north of To- were added to Alpinia, while later authors tended to refer kyo where the winters can be severe. Several species are im- American species to Renealmia L.f. Schumann (1904) ®nal- portant ornamentals (e.g., A. purpurata (Vieill.) K. Schum.) as ized these taxonomic concepts and subsequently Alpinia Roxb. potted plants, landscape accents, and cut ¯owers, and at least was conserved for the Asiatic species with Alpinia galanga one (A. zerumbet (Pers.) B.L. Burtt & R.M. Sm.) is naturalized (L.) Willd. as its type. in tropical regions around the world. In Asia, especially China Alpinia is the type genus of the tribe Alpinieae A. Rich. of (Wu and Larsen, 2000), alpinias are used as medicinals (e.g., the family Zingiberaceae. This tribe consists of evergreen A. of®cinarum Hance) and in cooking [A. galanga (L.) Willd.]. herbs, in which an abscission layer between the rhizome and Alpinias play an important ecological role in the understory the leafy shoots is lacking, the plane of distichy of the leaves of tropical and subtropical forests where many species are is transverse to the direction of growth of the rhizome, and quite common. In some cases (e.g., A. kwangsiensis T.L. Wu the lateral staminodes of the ¯owers are small, reduced to swellings at either side of the base of the labellum, or are 1 Manuscript received 26 March 2004; revision accepted 16 September entirely absent. Extra¯oral nectaries are absent, and the fruit 2004. The authors thank Ray Baker, Mike Bordelon, Jiang-Yun Gao, Mary Gibby, is usually spherical and indehiscent or ¯eshy (Kress et al., David Harris, Kai Larsen, Jing-Ping Liao, Ida Lopez, Achariya Rangsiruji, Chel- 2002). sea Specht, and Yong-Mei Xia, for discussion, assistance, and tissue samples Within the tribe Alpinieae, generic limits are dif®cult to dis- that made this investigation possible. This work was funded by the key project cern. While some genera may be easily recognized by their of the Ministry of Science and Technology of China (2001CCA00300), the respective morphological characters and/or geographic distri- National Natural Science Foundation of China Grants 30225007 and 30170069, the Smithsonian Scholarly Studies Program and the Biotic Surveys and Inven- bution (e.g., Aframomum, Elettaria, Hornstedtia, Burbidgea), tories Program of the National Museum of Natural History. it is hard to identify an apomorphy or universal character for 5 E-mail: [email protected]. species currently assigned to Alpinia. Virtually all species 167 168 AMERICAN JOURNAL OF BOTANY [Vol. 92 Figs. 1±9. Representative ¯oral types of the major groups of species of Alpinia. 1. Alpinia nigra. 2. A. galanga. 3. A. conchigera. 4. A. carolinensis. 5. A. zerumbet. 6. A. guangdongensis. 7. A. calcarata. 8. A. oxyphylla. 9. A. elegans. ¯ower terminally on the leafy shoots and all are Asiatic. These in¯orescence and ¯ower characters. Much variation exists in characters distinguish Alpinia from the Afro-American Re- these features (Figs. 1±9), from species with branched in¯o- nealmia, in which most species produce in¯orescences on a rescences and long cincinni subtended by bracts in which the separate, lea¯ess shoot from the rhizome, but do not uniquely ¯owers are each subtended by bracteoles, to other species with separate it from other members of the Alpinieae. Therefore, to no bracts or bracteoles and cincinni of only a single ¯ower. In a large degree, one is forced to recognize Alpinia only by the Flora of British India, Baker (1894) considered the species eliminating other genera, i.e., it is distinguished only by the of Alpinia that occur from Sri Lanka to Singapore. His account plesiomorphic characters of the tribe. included descriptions of 17 species from a known total of 30 Several attempts have been made to divide Alpinia into at that time and divided them into two subgenera and two smaller genera by elevating some of the more coherent groups sections according to the presence of an anther crest, the pos- of species to the generic rank. Holttum (1950) applied the session of large bracteoles, and the position of the in¯ores- name Alpinia to a small group of species with funnel-shaped cence. Schumann (1904) treated Alpinia throughout its range bracteoles and allocated the remaining species to Catimbium, in his account of the Zingiberaceae for Das P¯anzenreich (Ta- Cenolophon, and Languas. Several nomenclatural problems ble 1) dividing it into ®ve subgenera and 27 sections. Eight were present in this system, but its principal failing was that of Schumann's sections have now been placed in entirely dif- it only worked for the species of Malaysia. Later authors, ferent genera, leaving Alpinia with ®ve subgenera and 19 sec- therefore, returned to the concept of Alpinia sensu Schumann tions. Characteristics of the bracts and bracteoles are the most until Smith (1990) recognized a group of 22 species in New important diagnostic features in Schumann's classi®cation. Guinea that she segregated under the generic name Pleuran- Valeton (1913) later divided section Eubractea into subsection thodium (K. Schum.) R.M. Sm. Eustales and subsection Kolowratia and added a new section Infrageneric classi®cations of Alpinia have been based on Monanthocrater to Schumann's 1904 system. He admitted that January 2005] KRESS ET AL.ÐPHYLOGENY OF ALPINIA 169 TABLE 1. Infrageneric classi®cation of Alpinia according to Schumann (1904). Accepted generic Corresponding clades of Subgenus Section position molecular analyses Autalpinia Pycnopyramis 5 Plagiostachys Zerumbet (IV) Leptosolenia 5 Leptosolena Eubractea (V) Hellenia 5 Alpinia Galanga (II), Zerumbet (IV), Eubractea (V) Psychanthus 5 Pleuranthodium Tribe Riedelieae Cenolophon 5 Alpinia not represented Pleuranthodium 5 Pleuranthodium Tribe Riedelieae Guillania 5 Alpinia Eubractea (V) Probolocalyx 5 Alpinia Zerumbet (IV) Catimbium Flos Paradisi 5 Alpinia Zerumbet (IV) Boniophyton 5 Alpinia Zerumbet (IV) Dieramalpinia
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