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Systematics of Capparaceae and Cleomaceae: an Evaluation of the Generic Delimitations of Capparis and Cleome Using Plastid DNA Sequence Data1

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Systematics of Capparaceae and Cleomaceae: an Evaluation of the Generic Delimitations of Capparis and Cleome Using Plastid DNA Sequence Data1 682 Systematics of Capparaceae and Cleomaceae: an evaluation of the generic delimitations of Capparis and Cleome using plastid DNA sequence data1 Jocelyn C. Hall Abstract: The phylogenetic relationships in Capparaceae and Cleomaceae were examined using two plastid genes, ndhF and matK, to address outstanding systematic questions in the two families. Specifically, the monophyly of the two type genera, Capparis and Cleome, has recently been questioned. Capparaceae and Cleomaceae were broadly sampled to assess the generic circumscriptions of both genera, which house the majority of species for each family. Phylogenetic reconstruc- tions using maximum parsimony and maximum likelihood methods strongly contradict monophyly for both type genera. Within Capparaceae, Capparis is diphyletic: the sampled species belong to two of the five major lineages recovered in the family, which corresponds with their geographic distribution. One lineage contains all sampled New World Capparis and four other genera (Atamisquea, Belencita, Morisonia, and Steriphoma) that are distributed exclusively in the New World. The other lineage contains Capparis species from the Old World and Australasia, as well as the Australian genus, Apo- phyllum. Species of Cleome are scattered across each of four major lineages identified within Cleomaceae: (i) Cleome in part, Dactylaena, Dipterygium, Gynandropsis, Podandrogyne, and Polanisia;(ii) Cleome droserifolia (Forssk.) Del.; (iii) Cleome arabica L., and Cleome ornithopodioides L.; and (iv) Cleome in part, Cleomella, Isomeris, Oxystylis, and Wislizenia. Resolution within and among these major clades of Cleomaceae is limited, and there is no clear correspond- ence of clades with geographic distribution. Within each family, morphological support and taxonomic implications of the molecular-based clades are discussed. Key words: Capparaceae, Cleomaceae, Brassicaceae, cpDNA, chloroplast, phylogeny. Re´sume´ : Afin d’e´tudier les questions de syste´matique en suspens dans les familles des Capparaceae et des Cleomaceae, l’auteur a examine´ leurs relations phyloge´ne´tiques en utilisant deux ge`nes plastidiques, ndhF et matK.Re´cemment, on a spe´cifiquement remis en question la monophylie des deux genres types, Capparis et Cleome. L’auteur a largement e´chan- tillonne´ les Capparaceae et les Cleomaceae, afin de de´finir les circonscriptions de ces deux genres he´bergeant la majorite´ des espe`ces de chaque famille. Les reconstructions phyloge´ne´tiques a` l’aide des me´thodes de parcimonie et de probabilite´ maximale rejettent la monophylie pour les deux genres types. Chez les Capparaceae, Capparis est diphyle´tique; les espe`ces e´chantillonne´es appartiennent a` deux des cinq ligne´es principales de´couvertes pour la famille, lesquelles correspondent avec leur distribution ge´ographique. Une ligne´e contient tous les e´chantillons de Capparis du Nouveau Monde et quatre autres genres (Atamisquea, Belencita, Morisonia et Steriphoma) distribue´s exclusivement dans le Nouveau Monde. Les au- tres ligne´es contiennent des espe`ces de Capparis de l’Ancien monde et de l’Australasie ainsi que le genre australien Apo- phyllum. Les espe`ces de Cleome se re´partissent parmi les quatre ligne´es identifie´es au sein des Cleomaceae: (i) Cleome,en partie, Dactylaena, Dipterygium, Gynandropis, Podandrogyne et Polanisia;(ii) Cleome droserifolia;(iii) C. arabica et Cleome ornithopodioides L.; et (iv) Cleome, en partie, Cleomella, Isomeris, Oxystyli et Wislizenia.Lare´solution au sein et entre ces clades majeurs demeure limite´e et il n’y a pas de correspondance e´vidente des clades avec la distribution ge´ogra- phique. Pour chaque famille, l’auteur discute le support morphologique et les implications taxonomiques des clades base´s sur l’analyse mole´culaire. Mots-cle´s:Capparaceae, Cleomaceae, Brasicaceae, cpADN, chloroplaste, phyloge´nie. [Traduit par la Re´daction] Introduction lies Brassicaceae, Capparaceae, and Cleomaceae have high- lighted the lack of congruence between phylogeny and the As shown for many groups across the angiosperms, recent morphological characters that have been traditionally used molecular phylogenetic analyses of the closely related fami- in subfamilial, tribal, subtribal, and generic delimitations (Hall et al. 2002; Koch et al. 2003; Sa`nchez-Acebo 2005; Received 09 September 2007. Published on the NRC Research Al-Shehbaz et al. 2006; Beilstein et al. 2006). In addition, Press Web site at botany.nrc.ca on 25 June 2008. all three families have a high number of monotypic or di- J.C. Hall. Department of Biological Sciences, CW 405 typic genera, which are not especially helpful for reflecting Biological Sciences Building, University of Alberta, Edmonton, evolutionary relationships (Table 1; Al-Shehbaz et al. 2006). AB T6G 2E9, Canada (e-mail: [email protected]). Often, morphologically distinct small genera are embedded 1This paper is one of a selection of papers published in the within larger genera, leaving the larger genera nonmonophy- Special Issue on Systematics Research. letic. This pattern suggests that most, if not all, of these Botany 86: 682–696 (2008) doi:10.1139/B08-026 # 2008 NRC Canada Hall 683 Table 1. Species number (species sampled in current study) and geographic distribution of genera in Capparaceae and Cleomaceae. No. species Taxon (no. in current study) Distribution Capparaceaea s. str. Apophyllum F. Muell. 1 (1) Northeastern Australia Atamisquea Miers ex Hook. & Arn. 1 (1) South America, Mexico, and southwestern United States Bachmannia Pax 2 (0) Southern Africa Belencita H. Karst. 1 (1) Colombia Borthwickia W.W. Sm. 1 (0) Burma, China (Yunnan) Boscia Lam. 37 (3) Tropical and southern Africa, Arabia Buchholzia Engl. 2 (2) Western Africa Cadaba Forssk. 30 (2) Africa, Madagascar, Arabia, India, Malaysia to Australia Capparis L. 250 (27) Pantropical Cladostemon A. Braun & Vatke 1 (0) South and southeastern Africa Crateva L. 6 (3) Pantropical Dhofaria A.G. Mill. 1 (0) Arabia Euadenia Oliv. 3 (1) Tropical Africa Hypselandra Pax & K. Hoffm. 1 (0) Burma Maerua Forssk. 50 (2) Tropical and southern Africa to tropical Asia Morisonia L. 4 (1) Caribbean and tropical South America Ritchiea R. Br. ex G. Don 30 (1) Tropical and subtropical Africa Steriphoma Spreng. 8 (2) Tropical Americas Thylachium Lour. 10 (2) Eastern Africa and Madagascar Cleomaceae Buhsia Bunge 1 (0) Iran Cleome L. 200 (19) Pan- and sub-tropical Cleomella DC. 10 (2) Southwestern North America Dactylaena Schrad. ex Schult. f. 6 (2) West Indies and Brazil Dipterygium Decne. 1 (1) Egypt to Pakistan Gynandropsis DC. 1 (1) Africa, but pantropical weed (=Cleome gynandra L.) Haptocarpum Ule 1 (0) Eastern Brazil Isomeris Nutt. ex Torr. & Gray 1 (1) Southern North America and Mexico Oxystylis Torr. & Frem. 1 (1) Southwestern United States Podandrogyne Ducke 10 (3) Central America to Andes Polanisia Raf. 4 (1) North America (includes Cristatella Nutt.) Puccionia Chiov. 1 (0) Somalia Wislizenia Engelm. 1 (1) Southwestern North America aTribe Stixeae has been excluded; see Hall et al. (2004) and Kers (2003) small genera need to be sampled more intensively to gain a genera of both Capparaceae (Capparis L.) and Cleomaceae better understanding of phylogenetic relationships and ge- (Cleome L.). Presented herein is a plastid DNA (cpDNA) neric delimitations within these groups. Thus, to thoroughly phylogeny that represents the broadest taxon and the largest examine the monophyly of species-rich genera, numerous character sampling to date of Capparaceae and Cleomaceae monotypic and ditypic genera that are purported to be and that specifically addresses the generic limits of Capparis closely related must also be sampled. Of nearly equal impor- and Cleome. tance is the sampling of type species in molecular studies, Cleomaceae (13 genera, Table 1) are composed of three especially of species-rich genera, to contribute to the correct traditional subfamilies of Capparaceae s. l. (per Pax and formalization of nomenclatural changes that may result from Hoffmann 1936): Cleomoideae (9 genera: Cleome, Cleo- molecular analyses. Such a study has been undertaken for mella DC., Dactylaena Schrad. ex Schult. f., Gynandropsis the Brassicaceae, where a comprehensive family-level phy- DC., Haptocarpum Ule, Isomeris Nutt. ex Torr. & Gray, logeny included a large sampling of mono- and di-typic gen- Oxystylis Torr. & Frem., Polanisia Raf., and Wislizenia En- era (Beilstein et al. 2006), and it led to a re-classification of gelm.), Dipterygioideae (Dipterygium Decne.), Podandrogy- the family (Al-Shehbaz et al. 2006). However, sampling noideae (Podandrogyne Ducke), and unplaced genera strategies used in phylogenetic studies of Capparaceae and (Buhsia Bunge and Puccionia Chiov.). The close relation- Cleomaceae have not specifically addressed this issue. ship of Podandrogyne and Cleome has been proposed and Thus, while a better understanding of how the major clades widely accepted (Iltis 1958; Cochrane 1977). In contrast, of Capparaceae and Cleomaceae are related has emerged, Dipterygium has moved between Brassicaceae and Cappara- knowledge of generic and species relationships within these ceae s. l. (Hedge et al. 1980). Inclusion of Dipterygium in families remains poor, particularly for the species-rich type Cleomaceae is supported by molecular and chemical data # 2008 NRC Canada 684 Botany Vol. 86, 2008 (Hedge et al. 1980; Lu¨ning et al. 1992; Hall et al. 2002). based on a combined analysis of ndhF and trnL-trnF Even with the inclusion of other subfamilies, Cleomaceae
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