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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Molecular Phylogenetics and Evolution 57 (2010) 258–265 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Implications of a molecular phylogenetic study of the Malagasy genus Cedrelopsis and its relatives (Ptaeroxylaceae) Sylvain G. Razafimandimbison a,*, Marc S. Appelhans b,c, Harison Rabarison d, Thomas Haevermans e, Andriarimalala Rakotondrafara f, Stephan R. Rakotonandrasana f, Michel Ratsimbason f, Jean-Noël Labat e, Paul J.A. Keßler b,c, Erik Smets b,c,g, Corinne Cruaud h, Arnaud Couloux h, Milijaona Randrianarivelojosia i,j a Department of Botany, Bergius Foundation, Stockholm University, SE-10691, Stockholm, Sweden b Netherlands Centre for Biodiversity Naturalis (section NHN), Leiden University, 2300 RA, The Netherlands c Hortus Botanicus Leiden, Leiden, The Netherlands d Département de Biologie et Ecologie Végétales, Université d’Antananarivo, Madagascar e Muséum National d’Histoire Naturelle, Département Systématique et Evolution, UMR 7205 CNRS/MNHN Origine, Structure et Evolution de la Biodiversité, C.P. 39, 57 rue Cuvier, 75231 Paris Cedex 05, France f Centre National d’Application des Recherches Pharmaceutiques, BP 702, Antananarivo 101, Madagascar g Laboratory of Plant Systematics, Institute of Botany and Microbiology, K.U. Leuven, Kasteelpark Arenberg 31, BE-3001 Leuven, Belgium h Genoscope, Centre National de Sequençage, 2, rue Gaston Crémieux, CP5706, 91057 Evry Cedex, France i Unité de Recherche sur le Paludisme, Institut Pasteur de Madagascar, BP 1274, Antananarivo 101, Madagascar j School of Chemistry, University of KwaZulu-Natal, Durban 4041, South Africa article info abstract Article history: Ptaeroxylaceae is an Afro-Malagasy family containing three genera, Bottegoa, Cedrelopsis, and Ptaeroxylon. Received 12 January 2010 Although the family is morphologically well delimited, it is currently considered part of the subfamily Revised 15 June 2010 Spathelioideae in a broadly circumscribed orange family (Rutaceae). The Malagasy Cedrelopsis has tradi- Accepted 27 June 2010 tionally been associated with different families of the order Sapindales and its phylogenetic placement in Available online 30 June 2010 Rutaceae sensu lato has yet to be tested with molecular data. The present molecular phylogenetic study reaffirms the monophyly of Ptaeroxylaceae and its placement in Spathelioideae. Therefore, molecules and Keywords: morphology support close affinities between Bottegoa, Cedrelopsis, and Ptaeroxylon and also their current Biogeography generic circumscriptions. We report a case of an evolutionary change from one-seeded to two-seeded car- Bottegoa Cedrelopsis pels within the Harrisonia-Cneorum-Ptaeroxylaceae clade of Spathelioideae. Finally, the sister-group rela- Evolution of seed number tionship between the African Bottegoa and the Afro-Malagasy Ptaeroxylon-Cedrelopsis clade suggests an Ptaeroxylon African origin of Cedrelopsis. Ptaeroxylaceae Ó 2010 Elsevier Inc. All rights reserved. Rutaceae sensu lato Spathelioideae Sapindales 1. Introduction Many authors (e.g., APG II, 2003; APG III, 2009; Groppo et al., 2008) have adopted this concept of Rutaceae, although there seems The circumscription and infrafamilial classification of the or- to be no obvious morphological synapomorphy for it. Ptaeroxyla- ange family (Rutaceae) have been changed significantly based on ceae as presently circumscribed by Van der Ham et al. (1995) con- a series of independent molecular phylogenetic analyses (Gadek tains three genera: Bottegoa Chiov. (Chiovenda, 1916), Cedrelopsis et al., 1996; Chase et al., 1999; Scott et al., 2000; Poon et al., Baill. (Baillon, 1893), and Ptaeroxylon Eck. & Zeyh. (Ecklon and 2007; Groppo et al., 2008). Chase et al. (1999) recommended rec- Zeyher, 1835). The family was represented only by its type genus ognition of a broadly circumscribed Rutaceae, which includes the Ptaeroxylon in Gadek et al. (1996), Chase et al. (1999), and Groppo monogeneric Mediterranean family Cneoraceae sensu Oviedo et al. (2008). Within Rutaceae sensu lato, Harrisonia, Cneorum L., et al. (2009), the small Afro-Malagasy family Ptaeroxylaceae, and and Ptaeroxylaceae formed a clade together with two South Amer- the genus Harrisonia R.Br. ex A.Juss. of the family Simaroubaceae. ican rutaceous genera Dictyoloma A.Juss. and Spathelia L. (Gadek et al., 1996; Chase et al., 1999; Groppo et al., 2008). This clade, now recognized as subfamily Spathelioideae (Chase et al., 1999), * Corresponding author. Fax: +46 8 16 55 25. E-mail address: sylvain.razafi[email protected] (S.G. Razafimandim- is sister to a large clade containing the remaining members of bison). Rutaceae (hereafter called Rutaceae sensu stricto or the core 1055-7903/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2010.06.023 Author's personal copy S.G. Razafimandimbison et al. / Molecular Phylogenetics and Evolution 57 (2010) 258–265 259 Rutaceae). It is worth noting that Groppo et al. (2008) recently ceae as delimited by Van der Ham et al. (1995) based on morpho- suggested a formal recognition of these two sister lineages at sub- logical and phytochemical evidence is also supported by molecular familial level: subfamily Spathelioideae and subfamily Rutoideae, data from the coding chloroplast gene rbcL and two noncoding respectively. chloroplast markers, rps16 intron (Oxelman et al., 1997) and A large rbcL-based phylogenetic analysis of the Eudicots (Savo- trnL-F (Taberlet et al., 1991). The resulting phylogeny is used to as- lainen et al., 2000) resolved the monotypic African genera Bottegoa sess the evolution of seed number in the subfamily Spathelioideae and Ptaeroxylon as sisters (BS = 69) within a poorly supported and the biogeographic origin of Cedrelopsis. (BS = 50) subfamily Spathelioideae. This can be taken as an indica- tion of the monophyly of Ptaeroxylaceae sensu Van der Ham et al. 2. Materials and methods (1995); however, the third and largest genus of the family, Cedrel- opsis, was not investigated in that study. Van der Ham et al. (1995) 2.1. Taxon sampling and laboratory work postulated close relationships between the African Bottegoa, Cedrelopsis, and Ptaeroxylon based on some morphological, ana- Because Cedrelopsis has traditionally been associated with three tomical, and phytochemical features and transferred Bottegoa from families, namely Meliaceae, Ptaeroxylaceae, and Rutaceae, we sam- the family Sapindaceae to Ptaeroxylaceae, accordingly. Schatz pled 30 published rbcL sequences representing all recognized fam- (2001), recently supported by Groppo et al. (2008), transferred ilies in the order Sapindales sensu APG III (2009) and three the Malagasy Cedrelopsis from Ptaeroxylaceae to Rutaceae sensu outgroup taxa from the orders Brassicales, Malvales, and Picramni- lato on the basis of the close relationship between the African Bot- ales (Table 1). We sequenced one individual each of Cedrelopsis tegoa and Ptaeroxylon shown by Van der Ham et al. (1995) and grevei Baill. (type species of the genus), Cedrelopsis gracilis Savolainen et al. (2000) and their inclusion in Rutaceae as delim- J.-F. Leroy, and Cedrelopsis rakotozafyi Cheek & Lescot for the ited by Chase et al. (1999). The inclusion of Cedrelopsis based solely chloroplast coding gene rbcL according to the protocol outlined on morphological features raises a question as to whether or not in Razafimandimbison and Bremer (2002). The same specimens molecules and morphology are congruent regarding the close rela- of these species of Cedrelopsis, two specimens of Bottegoa insignis tionships among these genera, i.e., the monophyly of Ptaeroxyla- Choiv., one specimen of Harrisonia perforata Merr. were sequenced ceae sensu Van der Ham et al. (1995). The present study is the for the two chloroplast markers, rps16 intron and trnL-F, using the first to include all three genera of Ptaeroxylaceae sensu Van der primers published in Oxelman et al. (1997) and Taberlet et al. Ham et al. (1995) in the same molecular phylogenetic analysis. (1991), respectively (Table 1). These three chloroplast markers Cedrelopsis is a genus endemic to Madagascar comprising eight have been shown to be useful for assessing phylogenetic relation- species of dioecious or polygamous shrubs and small to large trees ships within the order Sapindales (e.g., Fernando et al., 1995; (Leroy and Lescot, 1990). The genus is distributed throughout the Gadek et al., 1996; Chase et al., 1999; Savolainen et al., 2000; dry deciduous forests and xerophyllous forests in Madagascar, Groppo et al., 2008). PCR was performed on a BioRad PTC200 with two species (Cedrelopsis procera J.-F. Leroy, and Cedrelopsis DNA Engine thermocycler. We amplified the rps16 and trnL-F ambanjensis J.-F. Leroy) restricted to semi-deciduous forests
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