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Systematics and Evolution of the Tropical Monocot Family Costaceae (Zingiberales): a Multiple Dataset Approach

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Systematics and Evolution of the Tropical Monocot Family Costaceae (Zingiberales): a Multiple Dataset Approach Systematic Botany (2006), 31(1): pp. 89±106 q Copyright 2006 by the American Society of Plant Taxonomists Systematics and Evolution of the Tropical Monocot Family Costaceae (Zingiberales): A Multiple Dataset Approach CHELSEA D. SPECHT1 Institute of Systematic Botany, New York Botanical Garden, Bronx, New York 10458 and Department of Biology, New York University, New York, New York 10003 1Current address: Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 ([email protected]) Communicating Editor: Lawrence A. Alice ABSTRACT. A phylogenetic analysis of molecular (ITS, trnL-F, trnK including the matK coding region) and morphological data is presented for the pantropical monocot family Costaceae (Zingiberales), including 65 Costaceae taxa and two species of the outgroup genus Siphonochilus (Zingiberaceae). Taxon sampling included all four currently described genera in order to test the monophyly of previously proposed taxonomic groups. Sampling was further designed to encompass geographical and morphological diversity of the family to identify trends in biogeographic patterns and morphological character evolution. Phylogenetic analysis of the combined data reveals three major clades with discrete biogeographic distribution: (1) South American, (2) Asian, and (3) African-neotropical. The nominal genus Costus is not monophyletic and its species are found in all three major clades. The Melanesian genus Tapeinochilos is monophyletic and included within the Asian clade. Monocostus and Dimerocostus are sister taxa and form part of the South American clade. The African-neotropical clade is composed entirely of the genus Costus; moreover, there is support for previously recognized subgeneric groupings within the Costus clade. Evolutionary trends in ¯oral morphology show that close associations with pollinators have evolved several times from an ancestral generalist pollinator ¯oral form. Bee pollination has evolved once in the family, arising in Africa from an open-¯owered (generalist) ancestor. Bird pollination has evolved multiple times: once from an open-¯owered ancestor in Southeast Asia and multiple times from a bee-pollinated ancestor in the neotropics. Additional morphological characters not traditionally used to de®ne taxonomic groups, but having high consistency in the current phylogenetic analysis, are discussed. Costaceae, a pantropical family of monocots con- on previous phylogenetic analysis of Costaceae, such sisting of approximately 120 species, is one of the most modi®cations of the tubular labellum for pollination easily recognizable groups within the order Zingiber- are derived, with an open labellum and hence a mor- ales. It is distinguished from other families including phology suggesting generalist pollination seemingly bananas (Musaceae) and gingers (Zingiberaceae) by its plesiomorphic within the family (Specht et al. 2001). well-developed and sometimes branched aerial shoots As presently circumscribed, the Costaceae compris- that have a characteristic spiral monistichous (one-sid- es four genera: Costus L. (ca. 95 spp., pantropical), ed) phyllotaxy (Kirchoff and Rutishauser 1990). The Monocostus K. Schum. (1 sp., Peru), Dimerocostus O. ¯oral structure of Costaceae is also unique within the Kuntz (3±5 spp., neotropical), and Tapeinochilos Miq. Zingiberales in that only a single fertile stamen devel- (18 spp., Melanesia). The genus Costus was divided by ops while the remaining ®ve infertile stamens fuse to- Schumann (1904) into ®ve subgenera (Costus, Epicostus, gether to form a large, petaloid labellum that domi- Metacostus, Paracostus,andCadalvena) based upon gen- nates the ¯oral display (Troll 1928; Kirchoff 1988). The eral characteristics of overall ¯oral morphology. Neo- labellum can be open or tubular, and when tubular can tropical species of subgenus Costus were placed by be modi®ed to accommodate either bee or bird polli- Maas (1979) into two sections based on labellum char- nation. When modi®ed for bee pollination, the tubular acteristics re¯ecting pollination syndromes: section labellum is largely white with a yellow central stripe Costus, with the tubular melittophilous labellum, and that acts as a nectar guide, leading bees to the nectary section Ornithophilus, with the tubular ornithophilous located at the base of the gynoecium. In these melit- labellum. A recent pollination study (Kay and Schem- tophilous taxa, the labellum is longer than the petals, ske 2003) demonstrated that the morphologically- forming a broad opening to the basal ¯oral tube. Re- based pollination syndromes identi®ed by Maas do re- ported bee pollinators include neotropical (Chrysanthe- ¯ect the preferred pollinators of the plants involved da, Euglossa, Eulaena, Euplusia,andExaerete)aswellas (bees for section Costus and birds for section Ornitho- pantropical (Anthophora, Lithurgus,andXylocopa)gen- philus). All neotropical taxa with the open labellum era. The labellum modi®ed for bird pollination is typ- and no apparent pollination af®liation were placed in ically red, orange, or dark yellow in color and is com- Costus subg. Cadalvena by Maas (1972, 1979) and Schu- monly contained within the petals, maintaining a rigid mann (1904). Epicostus (Africa), Metacostus (Africa), tubular structure. These ornithophilous taxa are polli- and Paracostus (Africa-Asia) were composed exclusive- nated by hummingbirds in the New World and by sun- ly of taxa with the open ¯oral form whereas subgenus birds in New Guinea and surrounding islands. Based Costus includes taxa with the melittophilous form in 89 90 SYSTEMATIC BOTANY [Volume 31 Africa and the open form in South East Asia in addi- subgenus Costus recognized by Maas (1977). Multiple exemplars were used in some cases to test monophyly of species or species tion to the neotropical ornithophilous and melittophil- complexes (e.g., Dimerocostus strobilaceus, Costus globosus, Costus ous forms described by Maas. speciosus). A previous phylogenetic analysis using molecular Character Sampling. Sampling of both morphological and mo- data (Specht et al. 2001) indicated that Tapeinochilos, lecular characters was attempted for each taxon included in the analysis with missing data present only in the molecular data. Monocostus,andDimerocostus are monophyletic but Inapplicable morphological characters for the outgroup (Siphono- Costus is polyphyletic. Within Costus, two of Schu- chilus) were designated as such in the morphological matrix and mann's subgenera (Epicostus and Metacostus) are par- were treated as missing in the analysis. The data matrix is avail- aphyletic to a larger clade that includes African and able upon request from the author. MORPHOLOGICAL CHARACTERS. Morphological characters for neotropical taxa placed in subgenus Costus. The Asian individual species were taken from the literature (Tomlinson 1962; members of subg. Costus form a clade sister to Tapeino- Koechlin 1964, 1965; Maas 1972, 1977, 1979; Maas and Maas van chilos making Costus subg. Costus polyphyletic. The de Kamer 1983; Lock 1985; Newman and Kirchoff 1992; Jaramillo and Kress 1997) where possible, with additional information gath- two species of subg. Cadalvena included in the analysis ered from direct observation in the ®eld and from living collec- are recovered as sister taxa and form part of a larger tions, alcohol-preserved material, and herbarium material. For the clade containing Monocostus and Dimerocostus. Because majority of characters, 3±7 exemplars were scored for each species only two species were used in the analysis, a robust included in the analysis. For characters that were found to be var- iable within species (indument, ¯ower color, bract length), poly- statement on the monophyly of subg. Cadalvena could morphisms were coded as multiple character states where appro- not be made. In addition, the type species of subg. priate (e.g., indument characters in Costus guanaiensis). For all spe- Cadalvena, Costus spectabilis from Africa, was not in- cies, including those where multiple exemplars were included for a single species (Costus globosus, Costus pulverulentus, Costus specio- cluded in the analysis. Finally, no representatives of sus,andDimerocostus strobilaceus), the same collections were used Schumann's subgenus Paracostus were included. for both DNA extraction and morphological character analysis. A The current analysis expands upon Specht et al. total of 71 characters were selected to include ¯oral, vegetative, (2001) by increasing the taxon and character sampling cytological, and anatomical structures, thereby enabling interpre- tation of morphological evolution within the family (Tomlinson to further test previous taxonomic delimitations within 1956, 1962). Attempts were made to reduce composite characters the family. The two species placed in Costus subg. Par- (i.e., pollination syndrome) to component structures (i.e., in¯ores- acostus (Schumann 1904) are included, as is the type of cence color, ¯oral shape) in order to maximize phylogenetic in- dependence and to avoid redundancy (Hawkins et al. 1997; Poe subg. Cadalvena and several additional African species and Wiens 2000). Characters and character states are listed in Ap- placed by Schumann in subgenera Metacostus and Epi- pendix 1. costus. Character sampling was increased with two ad- Ovary structure (character numbers 28±36) was studied as de- ditional DNA sequence regions and a 71 character tailed by Newman and Kirchoff (1992) and an attempt was made to adhere to criteria established therein.
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