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Richard G. Olmstead, 2,6 Michelle L. Zjhra, 3,7 L Ú Cia G. Lohmann, 4,8

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Richard G. Olmstead, 2,6 Michelle L. Zjhra, 3,7 L Ú Cia G. Lohmann, 4,8 American Journal of Botany 96(9): 1731–1743. 2009. A MOLECULAR PHYLOGENY AND CLASSIFICATION OF BIGNONIACEAE 1 Richard G. Olmstead, 2,6 Michelle L. Zjhra, 3,7 L ú cia G. Lohmann, 4,8 Susan O. Grose, 2 and Andrew J. Eckert 2,5 2 Department of Biology, University of Washington, Seattle, Washington 98195 USA; 3 Department of Biology, Box 8042, Georgia Southern University, Statesboro, Georgia 30460 USA; 4 Department of Biology, University of University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121 USA; and 5 Section of Evolution and Ecology, University of California at Davis, One Shields Avenue, Davis, California 95616 USA Bignoniaceae are woody, trees, shrubs, and lianas found in all tropical fl oras of the world with lesser representation in temperate regions. Phylogenetic analyses of chloroplast sequences ( rbcL , ndhF , trnL-F ) were undertaken to infer evolutionary relationships in Bignoniaceae and to revise its classifi cation. Eight clades are recognized as tribes (Bignonieae, Catalpeae, Coleeae, Crescen- tieae, Jacarandeae, Oroxyleae, Tecomeae, Tourrettieae); additional inclusive clades are named informally. Jacarandeae and Catal- peae are resurrected; the former is sister to the rest of the family, and the latter occupies an unresolved position within the “ core ” Bignoniaceae. Tribe Eccremocarpeae is included in Tourrettieae. Past classifi cations recognized a large Tecomeae, but this tribe is paraphyletic with respect to all other tribes. Here Tecomeae are reduced to a clade of approximately 12 genera with a worldwide distribution in both temperate and tropical ecosystems. Two large clades, Bignonieae and Crescentiina, account for over 80% of the species in the family. Coleeae and Crescentieae are each included in larger clades, the Paleotropical alliance and Tabebuia al- liance, respectively; each alliance includes a grade of taxa assigned to the traditional Tecomeae. Parsimony inference suggests that the family originated in the neotropics, with at least fi ve dispersal events leading to the Old World representatives. Key words: Bignoniaceae; biogeography; chloroplast DNA; classifi cation; molecular systematics; ndhF ; phylogeny; rbcL ; trnL-F . This paper is dedicated to the memory of Al Gentry, Bignoni- opted a herbaceous habit, mostly at high elevations in the Hima- aceae scholar; without his tremendous energy and insights, this laya ( Incarvillea ) and the Andes ( Argylia , Tourrettia ). Several study would not have been possible. genera include species of horticultural importance in tropical and temperate regions, including Bignonia , Campsis , Catalpa , Bignoniaceae are predominantly a neotropical family and are Jacaranda , Spathodea , and Tabebuia. Relatively few species an important component of neotropical forests, with lesser con- have economic signifi cance outside horticulture, but numerous tributions to African, Malagasy, and SE Asian tropical forests. species have been used by indigenous peoples for food, timber, The family includes 82 genera and 827 species ( Lohmann and containers, medicinal, and ritual purposes ( Gentry, 1992c ). Ulloa, 2007 ). Approximately half of both genera and species Bignoniaceae belong in Lamiales ( Olmstead et al., 1993 ; belong to the New World endemic tribe Bignonieae, which Angiosperm Phylogeny Group, 2003 ), where their closest rela- comprise a major component of the neotropical liana fl ora. Most tives are unclear ( Olmstead et al., 2001 ; Oxelman et al., 2005 ). A other species are woody shrubs and trees, including savannah group of small genera including Schlegelia often has been placed and tropical forest canopy trees, although three groups have ad- in Bignoniaceae ( Armstrong, 1985 ) as tribe Schlegelieae ( Gentry, 1980 ). However, phylogenetic evidence for this rela- tionship is equivocal, with some studies fi nding a weakly sup- 1 Manuscript received 2 January 2009; revision accepted 9 April 2009. ported sister group relationship with Bignoniaceae s.s. (e.g., The authors thank the curators and staff of the herbaria GH, MO, UC, Olmstead et al., 2001 ) and others placing Schlegelieae else- US and botanical gardens Jardin Botanico Nacional de Cuba, Huntington where, though nearby, on the phylogenetic tree ( Spangler and Botanical Gardens, Matthaei Botanical Gardens, Missouri Botanical Olmstead, 1999 ; Bremer et al., 2002 ; Oxelman et al., 2005 ). Garden, Royal Botanic Gardens Edinburgh, Royal Botanic Gardens Kew, University of California Botanical Garden, and Waimea Botanical Garden Without strong support for a clade comprising Bignoniaceae s.s. for providing material for this research. They also thank M. Chase, J. Clark, and Schlegelieae, it is appropriate to classify them separately G. dos Santos, D. Folsom, A. Gentry, and G. Schatz for assistance in ( Reveal, 1996 ; APG II, 2003). Paulownia also is sometimes con- obtaining material and P. Reeves for assistance in the laboratory. This work sidered close to Bignoniaceae ( Armstrong, 1985 ), but this rela- was supported by NSF grants DEB-9509804, DEB-9727025, and DEB- tionship is rejected by all phylogenetic studies currently available 0309065 to R.G.O. and S.O.G.; NSF grants DEB-9423577, DBI-9804155, (e.g., Spangler and Olmstead, 1999 ; Olmstead et al., 2001 ; and DBI-IBN-0107907 to M.L.Z.; and NSF grant DEB-0073052 to L.G.L. Bremer et al., 2002 ). Hence, Paulownia also is placed in its own 6 Author for correspondence ( [email protected] ) small family Paulowniaceae ( Nakai, 1949 ; APG II, 2003). 7 Present address: Dean of Undergraduate Studies, Asian University for The taxonomic history of the family was described in detail Women, AUW Support Foundation, 1100 Massachusetts Ave., Suite 300, by Gentry (1980) and summarized by Spangler and Olmstead Cambridge, Massachusetts 02138 USA 8 Present address: Universidade de São Paulo, Instituto de Biociências, (1999) . The most recent classifi cation of Bignoniaceae by Departamento de Botânica, Caixa Postal 11461 05422-970, São Paulo, SP, Fischer et al. (2004) recognized seven of the eight tribes pro- Brasil posed by Gentry (1980) : Bignonieae, Coleeae, Crescentieae, Eccremocarpeae, Oroxyleae, Tecomeae, and Tourrettieae. Only doi:10.3732/ajb.0900004 Schlegelieae were excluded from this treatment. 1731 1732 American Journal of Botany [Vol. 96 Phylogenetic and monographic studies focusing on clades Tabebuia alliance ( Grose and Olmstead, 2007a ). This clade is within Bignoniaceae have revised tribal and generic boundaries characterized by palmately compound leaves (or a derivative and species numbers for several groups, including Coleeae unifoliate condition) and was recognized by Bentham and ( Zjhra et al., 2004 ), Bignonieae ( Lohmann, 2006 , in press ), In- Hooker (1876) as the informal group Digitifolieae. Further- carvillea ( Chen et al., 2005 ), Crescentieae/ Tabebuia s.l. ( Grose more, Crescentieae are nested within the large neotropical ge- and Olmstead, 2007a , b ), and Catalpa ( Li, 2008 ). Taking these nus Tabebuia , requiring that Tabebuia be split into three genera: recent studies into account, along with the two-volume mono- Handroanthus , Roseodendron , and Tabebuia ( Grose and Olm- graph of neotropical Bignoniaceae ( Gentry, 1980 , 1992a ), the stead, 2007b ). portions of the family that remain most poorly known are the The classifi cation of tribe Bignonieae traditionally has con- African and Asian groups, which account for approximately 29 sisted of a few large genera and many small ones, with many genera and 115 species ( Lohmann and Ulloa, 2007 ). problematic generic delimitations (Lohmann, 2006). A com- Previous phylogenetic studies have provided an outline of bined cpDNA and nuclear DNA study of Bignonieae ( Lohm- relationships in the family. However, these studies have lacked ann, 2006 ) with nearly one-third of the species sampled, sorted much detail due to limited sampling for many lineages. A pre- out many of the problems of generic delimitation and resulted liminary study of the family using the chloroplast DNA (cp- in a revised classifi cation of Bignonieae in which the 47 genera DNA) genes rbcL and ndhF ( Spangler and Olmstead, 1999 ) traditionally recognized in the tribe are reduced to 21 ( Lohm- found that the monophyly of Bignoniaceae itself was only ann, in press ). weakly supported, with confl ict between the two DNA regions Other, fi ne-scale, species-level phylogenetic studies in Bi- with respect to its monophyly. The lack of strong molecular gnoniaceae have been few. Chen et al., (2005) used a combined evidence for monophyly contrasts with the consistent recogni- cpDNA ( trnL-F ) and ITS approach to understand species rela- tion of Bignoniaceae in all previous classifi cations (apart from tionships in Chinese Incarvillea , and Li (2008) used ndhF and the debate over Paulownia and Schlegelieae). Bignoniaceae are ITS to resolve relationships in the North American and Asian easily recognized by a suite of vegetative and reproductive Catalpa . characters, including woody habit (except the herbaceous Ar- This study integrates results from three studies that focused gylia , Incarvillea , and Tourrettia ), usually opposite and com- on major clades of Bignoniaceae (Bignonieae: Lohmann, 2006; pound leaves, bilabiate fl owers mostly with four stamens and a Coleeae: Zjhra et al., 2004; Crescentieae and the Tabebuia alli- staminode, and usually dehiscent, capsular fruits splitting along ance: Grose and Olmstead, 2007a), with data from representa- two sutures and containing winged seeds (except the indehis- tive sampling of the
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