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Bremer Et Al. 2001 Plant Syst. Evol. 229: 137±169 <2001) A phylogenetic analysis of 100+ genera and 50+ families of euasterids based on morphological and molecular data with notes on possible higher level morphological synapomorphies K. Bremer1, A. Backlund2, B. Sennblad3, U. Swenson4, K. Andreasen5, M. Hjertson1, J. Lundberg1, M. Backlund1, and B. Bremer1 1Department of Systematic Botany, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden 2Department of Medicinal Chemistry, Uppsala University, Uppsala, Sweden 3Stockholm Bioinformatics Center, Stockholm University, Stockholm, Sweden 4Department of Botany, University of Stockholm, Stockholm, Sweden 5Molecular Systematics Laboratory, Swedish Museum of Natural History, Stockholm, Sweden Received August 28, 2000 Accepted August 7, 2001 Abstract. A data matrix of 143 morphological and epigynous ¯owers, ``late sympetaly'' with distinct chemical characters for 142 genera of euasterids petal primordia, free stamen ®laments, and indehi- according to the APG system was compiled and scent fruits. It is unclear which of these characters complemented with rbcL and ndhF sequences for represent synapomorphies and symplesiomorphies most of the genera. The data were subjected to for the two groups, respectively, and there are parsimony analysis and support was assessed by numerous expections to be interpreted as reversals bootstrapping. Strict consensus trees from analyses and parallelisms. of morphology alone and morphology + rbcL+ ndhF are presented. The morphological data re- Key words: Angiosperms, asterids, euasterids, cover several groups supported by molecular data Asteridae, Apiales, Aquifoliales, Asterales, but at the level of orders and above relationships Dipsacales, Garryales, Gentianales, Lamiales, are only super®cially in agreement with molecular Solanales, Adoxaceae. Cladistics, phylogeny, studies. The analyses provide support for mono- morphology, rbcL, ndhF. phyly of Gentianales, Aquifoliales, Apiales, Aste- rales, and Dipsacales. All data indicate that Asterids comprise more that 1/4 of the ¯ow- Adoxaceae are closely related to Dipsacales and ering plants <Bremer et al. 2000). They are hence they should be included in that order. The often herbaceous plants with sympetalous trees were used to assess some possible morpho- corollas and stamens in one series. In the logical synapomorphies for euasterids I and II and classi®cation by the Angiosperm Phylogeny for the orders of the APG system. Euasterids I are Group <APG 1998), which will be followed generally characterised by opposite leaves, entire here, asterids are grouped in ten orders, viz. leaf margins, hypogynous ¯owers, ``early sympe- taly'' with a ring-shaped corolla primordium, Cornales Dumort., Ericales Dumort., Garry- fusion of stamen ®laments with the corolla tube, ales Lindl., Gentianales Lindl., Solanales and capsular fruits. Euasterids II often have Dumort., Lamiales Bromhead, Aquifoliales alternate leaves, serrate-dentate leaf margins, Senft, Apiales Nakai, Dipsacales Dumort., and 138 K. Bremer et al.: Phylogenetic analysis of euasterids Asterales Lindl. The last eight of these consti- et al. 1993) or euasterids I and II <APG 1998), tute the euasterids. Asterids are traditionally corresponding to I) Garryales, Gentianales, known as Sympetalae Rchb., because of the Lamiales, and Solanales, and II) Apiales, sympetalous corollas. Sympetalous plants were Aquifoliales, Asterales, and Dipsacales. Sub- conceived as a group already in the 17th sequently circumscription of the asterids has century and they are more or less consistently been complemented by analyses of extended recognised in ¯owering plant classi®cation ever rbcL, ndhF, atpB, and 18S rDNA data sets since Jussieu 1789 <Wagenitz 1992). Takhtajan with more taxa including whole families re- <1964, 1969) renamed the group as subclass vealed to belong among the asterids <Savolai- Asteridae Takht., although he <Takhtajan nen et al. 1994; Hempel et al. 1995; Gustafsson 1987, 1997) later restricted Asteridae to the et al. 1996; Morton et al. 1996; Plunkett et al. core of Asterales as currently understood 1996; Backlund and Bremer 1997; Soltis and <APG 1998) and placed the other orders in a Soltis 1997; Soltis et al. 1997; Backlund et al. subclass Lamiidae Takht. ex Reveal. Before 2000; Olmstead et al. 2000; Savolainen et al. the 1990s <e.g. Cronquist 1981), Asteridae 2000a, b; Soltis et al. 2000). Jackknife and generally comprised plants now classi®ed in bootstrap analyses have corroborated mono- Gentianales, Solanales, Lamiales, Dipsacales, phyly of asterids, euasterids, euasterids I and and Asterales. Parts of Ericales were earlier II, and the 10 orders recognised by APG considered members of Sympetalae but they <1998). In particular, there is the large jack- were excluded from Asteridae by Takhtajan knife analysis of the rbcL gene from 2538 green <1964, 1969). Many groups outside Asteridae plants by KaÈ llersjoÈ et al. <1998), jackknife have been considered their close relatives and analysis of the rbcL and atpB genes from 357 potential candidates for inclusion among the ¯owering plants by Savolainen et al. <2000a), asterids. Mainly due to the presence of poly- bootstrap analysis of the 18S rDNA, rbcL and acetylenes and iridoids, Dahlgren <1989) thus atpB genes from 190 ¯owering plants by Soltis placed Apiales <=Araliales Reveal) and Cor- et al. <1998), and jackknife analysis of the nales <including many families now in other same three genes from 545 ¯owering plants by asterid orders ) close to Asterales and Dipsa- Soltis et al. <2000). cales, respectively, and in Dahlgren's diagrams There have been comparatively few at- Ericales were surrounded by Cornales, Dipsa- tempts at reconstructing higher-level <suprafa- cales, Gentianales, Lamiales, and Solanales. milial and supraordinal) interrelationships of However, it was not until the breakthrough of ¯owering plants by cladistic analysis of mor- molecular information in 1992 and 1993 phological data. No doubt this is due to the <Olmstead et al. 1992, 1993; Downie and complex nature of constructing morphological Palmer 1992; Chase et al. 1993) that asterids data matrices. Assembling a morphological became more widely circumscribed. data matrix of, say, 100 families and 150 With cladistic analysis of nucleotide characters is normally a much more dicult sequences from the rbcL gene of the chloro- enterprise than sequencing the rbcL gene from plast genome, it soon became evident that the 100 species. Huord <1992) made a morpho- traditional Asteridae <approximately Gentia- logical cladistic analysis of nearly 70 mostly nales, Lamiales, Solanales, Asterales, Dipsa- rosid but also some asterid families. His trees cales) are nested in a larger monophyletic show many similarities with the well-supported group including also Cornales, Ericales, phylogenies obtained from the molecular data. Garryales, Apiales, and Aquifoliales <Olm- However, there are also several gross discrep- stead et al. 1992, 1993, where they are some- ancies. For example, the asterid Apiales are in what dierently named). It also became Huord's trees nested in the rosid Malpighiales evident that there are two major subgroups Mart., illustrating the diculties with morpho- of asterids, known as Asterid I and II <Chase logical data at higher taxonomic levels. The K. Bremer et al.: Phylogenetic analysis of euasterids 139 morphological data are no more homoplastic ical synapomorphies for the major euasterid than the molecular data, but the number of groups of the APG system. informative characters is much lower and their pattern of variation is much more complex Material and methods <e.g. Bremer et al. 1999). This is illustrated also by the large analysis of Nandi et al. <1998). Terminal taxa. The data matrix comprises 142 They analysed non-molecular <morphological, genera of euasterids. Their classi®cation into fam- chemical, and serological) and rbcL data from ilies, orders, and the two major groups of euasterids 161 ¯owering plant taxa <families and various I and euasterids II is shown in Appendix 1 suprafamilial taxa), among them 1/4 asterids following APG <1998). In general, we have sampled more genera from large and morphologically including 14 euasterids <Asterids I and II). complex families. Many families are represented Nandi et al.'s morphological trees are similar by a single genus, in many cases simply because the to the molecular-derived phylogenies but family is monogeneric. All morphological charac- again, as in Huord's <1992) morphological ters refer to the genus. If there is variation within trees, there are considerable discrepancies. the genus for a particular character, this is treated Nandi et al.'s bootstrap analyses of their data as discussed below under morphological data. We set also reveal very weak support for the have chosen genera as terminal taxa rather than morphological trees. Other morphological species or families. With species, the morphological cladistic analyses involving several families variation in the data matrix would have been very of asterids are mostly restricted to single orders sensitive to the taxon sampling, i.e. the particular or groups of families. Anderberg <1992, 1993) species that happen to be included, and the results analysed Ericales sensu stricto, Struwe et al. would be heavily dependent on the sampling. With families as terminal taxa, the problems of morpho- <1994) analysed Gentianales, Anderberg and logical variation within the families and how to StaÊ hl <1995) Primulales Dumort. <now part of code
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