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Phylogeny and Classification of Ranunculales: Evidence from Four ARTICLE IN PRESS Perspectives in Plant Ecology, Evolution and Systematics Perspectives in Plant Ecology, Evolution and Systematics 11 (2009) 81–110 www.elsevier.de/ppees Phylogeny and classification of Ranunculales: Evidence from four molecular loci and morphological data Wei Wanga, An-Ming Lua, Yi Renb, Mary E. Endressc, Zhi-Duan Chena,Ã aState Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, 20 Nanxincun, Xiangshan, Beijing 100093, PR China bKey Laboratory of Medicinal Plant Resource and Natural Pharmaceutical Chemistry of Ministry of Education, College of Life Sciences, Shaanxi Normal University, Xi’an 710062, PR China cInstitute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland Received 30 June 2008; received in revised form 21 November 2008; accepted 5 January 2009 Abstract Previous phylogenetic analyses of Ranunculales, which have mostly been focused on an individual family and were based on molecular data alone, have recovered three main clades within the order. However, support for relationships among these three clades was weak. Earlier hypotheses were often hampered by limited taxon sampling; to date less than one-tenth of the genera in the order have been sampled. In this study, we used a greatly enlarged taxon sampling (105 species, representing 99 genera of all seven families in the order). Our study is, furthermore, the first to employ morphology (65 characters) in combination with sequence data from four genomic regions, including plastid rbcL, matK and trnL-F, and nuclear ribosomal 26S rDNA to reconstruct phylogenetic relationships within Ranunculales. Maximum parsimony and Bayesian inference were performed on the individual and combined data sets. Our analyses concur with those of previous studies, but in most cases provide stronger support and better resolution for relationships among the three main clades retrieved. The first, comprised solely of the monogeneric family Eupteleaceae, is the earliest-diverging lineage. The second clade is composed exclusively of taxa of Papaveraceae, which is sister to the third clade, the core Ranunculales, comprising the other five families of the order. Circaeasteraceae and Lardizabalaceae form a strongly supported clade. Pteridophyllum is supported as sister to Hypecoum, contradicting the viewpoint that the former is the earliest-diverging genus in Papaveraceae. Glaucidium is basalmost in Ranunculaceae. Within this phylogenetic framework, the evolution of selected characters is inferred and diagnostic morphological characters at different taxonomic levels are identified and discussed. Based on both morphological and molecular evidence, a classification outline for Ranunculales is presented, including the proposal of two new subfamilies, Menispermoideae and Tinosporoideae in Menispermaceae and a new tribe, Callianthemeae, for the genus Callianthemum (Ranunculaceae). r 2009 Ru¨bel Foundation, ETH Zu¨rich. Published by Elsevier GmbH. All rights reserved. Keywords: Bayesian inference; Combined molecular and morphological data; Diagnostic characters; Parsimony analysis; Phylogenetic relationships of Ranunculales ÃCorresponding author. Tel.: +86 10 62836434; fax: +86 10 62590843. E-mail address: [email protected] (Z.-D. Chen). 1433-8319/$ - see front matter r 2009 Ru¨bel Foundation, ETH Zu¨rich. Published by Elsevier GmbH. All rights reserved. doi:10.1016/j.ppees.2009.01.001 ARTICLE IN PRESS 82 W. Wang et al. / Perspectives in Plant Ecology, Evolution and Systematics 11 (2009) 81–110 Introduction phylogenetic methods, have produced conflicting topo- logies that are in part only weakly supported (e.g., Hoot The order Ranunculales is recognized in many and Crane, 1995; Hoot et al., 1999; Qiu et al., 2005, classification systems (e.g., Hutchinson, 1973; Dahlgren, 2006; Savolainen et al., 2000a, b; Soltis et al., 2000, 2003; 1983; Cronquist, 1988; Kubitzki et al., 1993; Takhtajan, Nickrent et al., 2002; Hilu et al., 2003; Zanis et al., 2003; 1997; APG, 1998; Wu et al., 2002; APG II, 2003; Kim et al., 2004a; Worberg et al., 2007). Furthermore, Thorne, 2007); however, its circumscription has long the weakly supported sister relationship identified been controversial. Dahlgren’s (1983) Ranunculales between Circaeasteraceae and Lardizabalaceae (Hoot included Ranunculaceae (excluding Glaucidium), Lardi- and Crane, 1995; Hoot et al., 1999; Savolainen et al., zabalaceae, Menispermaceae, Berberidaceae, Circaeast- 2000a; Soltis et al., 2003; Kim et al., 2004a) needs eraceae, and several segregate families, such as reevaluation. Kingdoniaceae, Sargentodoxaceae, Fumariaceae, and Several monotypic genera within the order, such as Glaucidiaceae. In addition to the nine families above, Glaucidium, Hydrastis, Kingdonia, Nandina, Pteridophyl- Cronquist (1988) added Sabiaceae and Coriariaceae, lum, and Sargentodoxa, differ in their position and and Kubitzki et al. (1993) and Thorne (2007) merged taxonomic rank among the different classification Dahlgren’s (1983) Papaverales into the order. In systems. For example, Glaucidium has been placed in contrast, Takhtajan’s (1997) and Wu et al.’s (2002) Ranunculaceae (e.g., Hutchinson, 1973; Dahlgren, 1980; Ranunculales contained only the family Ranunculaceae Cronquist, 1988), in Hydrastidaceae (Tobe, 2002), or (excluding Hydrastis and Glaucidium). given familial rank and positioned close to Paeoniaceae Molecular phylogenetics has contributed greatly to or Paeoniales (e.g., Takhtajan, 1997; Wu et al., 2002; the delimitation of the Ranunculales over the past Thorne, 2007). The taxonomic contention involving decade. Based on chloroplast rbcL sequences, Chase these genera is the basis of the dispute over the et al. (1993) first recovered a clade (labeled ‘‘Ranuncu- delimitation of the order Ranunculales as well as that lids’’), which contained Berberidaceae, Eupteleaceae, of some of its constituent families. Recent broad-based Lardizabalaceae, Menispermaceae, Papaveraceae sensu phylogenetic analyses in angiosperms or eudicots have lato (including Fumariaceae), and Ranunculaceae. The placed each of these monotypic genera into a family; inclusion of Euptelea in the ranunculids was surprising, however, their positions have not been sufficiently as it has traditionally been placed among the ‘‘lower’’ clarified due to the relatively limited taxon sampling in hamamelids. However, the same ‘‘Ranunculids’’ clade each family. Analyses focusing on selected families in was recovered by 18S rDNA sequence analysis (Soltis the Ranunculales, such as Berberidaceae (Kim and et al., 1997), and this in turn was congruent with results Jansen, 1996, 1998; Kim et al., 2004b; Wang et al., from a study using three gene data by Hoot and Crane 2007a), Lardizabalaceae (Hoot et al., 1995; Wang et al., (1995), which also added Circaeasteraceae (including 2002), Papaveraceae (Hoot et al., 1997), and Ranuncu- Kingdonia) to the clade. Subsequent analyses have laceae (Johansson and Jansen, 1993; Hoot, 1995; supported seven families in Ranunculales: Berberidaceae Johansson, 1995; Kosuge et al., 1995; Ro et al., 1997), (including Nandinaceae), Circaeasteraceae (including resolved the positions of some of these monotypic Kingdoniaceae), Eupteleaceae, Lardizabalaceae (includ- genera, however, in most cases, did not follow through ing Sargentodoxaceae), Menispermaceae, Papaveraceae with the taxonomic consequences. (including Fumariaceae and Pteridophyllaceae), and There exists a striking disproportion in species Ranunculaceae (including Glaucidiaceae and Hydrasti- number among the families in the order. At one end daceae) (APG, 1998 ; Hoot et al., 1999; Savolainen of the spectrum are Circaeasteraceae and Eupteleaceae, et al., 2000a; Soltis et al., 2000, 2003; APG II, 2003; Kim each with only two species; Lardizabalaceae contains 50, et al., 2004a). Menispermaceae 450, Berberidaceae ca. 650 and Papa- The Ranunculales sensu APG II (2003) is a strongly veraceae 750 species. At the other end of the spectrum supported monophyletic group within basal eudicots, are Ranunculaceae, with some 2000 species. Of the ca. which are sister to all other eudicots (Chase et al., 1993; 200 genera in Ranunculales, less than 20 genera have Savolainen et al., 2000b; Soltis et al., 1997, 2000; Hilu been sampled in previous studies (e.g., Chase et al., et al., 2003). The consensus is that the order comprises 1993; Hoot and Crane, 1995; Soltis et al., 1997, 2000, three main constituent clades: the two earlier-diverging 2003; Hoot et al., 1999; Savolainen et al., 2000a, b; Hilu ranunculids Eupteleaceae and Papaveraceae on the one et al., 2003; Kim et al., 2004a; Worberg et al., 2007). hand, and the well-supported clade of core Ranuncu- Thus to date the patterns of morphological character lales, consisting of the other five families, which is more evolution in Ranunculales have not been sufficiently derived, on the other (see Kim et al., 2004a). The well elucidated. In particular, the morphological syna- relationship among these three clades, however, remains pomorphies that define Ranunculales are still unclear. uncertain, because previous analyses, employing The objectives of this study are (1) to investigate different taxon and character sampling schemes and the phylogenetic relationships at generic level within ARTICLE IN PRESS W. Wang et al. / Perspectives in Plant Ecology, Evolution and Systematics 11 (2009) 81–110 83 Ranunculales using four molecular loci from the as missing or inapplicable. The complete character chloroplast and
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