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Comparative Floral Structure and Systematics in Rhizophoraceae

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Comparative Floral Structure and Systematics in Rhizophoraceae Botanical Journal of the Linnean Society, 2011, 166, 331–416. With 197 figures Comparative floral structure and systematics in Rhizophoraceae, Erythroxylaceae and the potentially related Ctenolophonaceae, Linaceae, Irvingiaceae and Caryocaraceae (Malpighiales) Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 MERRAN L. MATTHEWS* and PETER K. ENDRESS FLS Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, CH-8008 Zurich, Switzerland Received 28 January 2011; revised 3 May 2011; accepted for publication 27 May 2011 Within the rosid order Malpighiales, Rhizophoraceae and Erythroxylaceae (1) are strongly supported as sisters in molecular phylogenetic studies and possibly form a clade with either Ctenolophonaceae (2) or with Linaceae, Irvingiaceae and Caryocaraceae (less well supported) (3). In order to assess the validity of these relationships from a floral structural point of view, these families are comparatively studied for the first time in terms of their floral morphology, anatomy and histology. Overall floral structure reflects the molecular results quite well and Rhizo- phoraceae and Erythroxylaceae are well supported as closely related. Ctenolophonaceae share some unusual floral features (potential synapomorphies) with Rhizophoraceae and Erythroxylaceae. In contrast, Linaceae, Irvingiaceae and Caryocaraceae are not clearly supported as a clade, or as closely related to Rhizophoraceae and Erythroxy- laceae, as their shared features are probably mainly symplesiomorphies at the level of Malpighiales or a (still undefined) larger subclade of Malpighales, rather than synapomorphies. Rhizophoraceae and Erythroxylaceae share (among other features) conduplicate petals enwrapping stamens in bud, antepetalous stamens longer than antesepalous ones, a nectariferous androecial tube with attachment of the two stamen whorls at different positions: one whorl on the rim, the other below the rim of the tube, the ovary shortly and abruptly dorsally bulged and the presence of a layer of idioblasts (laticifers?) in the sepals and ovaries. Ctenolophonaceae share with Rhizophoraceae and/or Erythroxylaceae (among other features) sepals with less than three vascular traces, a short androgynophore, an ovary septum thin and severed or completely disintegrating during development, leading to a developmentally secondarily unilocular ovary, a zigzag-shaped micropyle and seeds with an aril. Special features occurring in families of all three groupings studied here are, for example, synsepaly, petals not retarded and thus forming protective organs in floral bud, petals postgenitally fused or hooked together in bud, androecial tube and petals fusing above floral base, androecial corona, apocarpous unifacial styles, nucellus thin and long, early disintegrating (before embryo sac is mature), and nectaries on the androecial tube. Some of these features may be synapomorphies for the entire group, if it forms a supported clade in future molecular studies, or for subgroups thereof. Others may be plesiomorphies, as they also occur in other Malpighiales or also in Celastrales or Oxalidales (COM clade). The occurrence of these features within the COM clade is also discussed. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416. ADDITIONAL KEYWORDS: androecium – Celastrales – COM clade – core eudicots – floral anatomy – floral morphology – gynoecium – malvids – Oxalidales – perianth – rosids. INTRODUCTION large clade based on molecular phylogenetic studies, containing newly found orders and orders with The present study is part of a series of comparative largely new family compositions (e.g. Chase et al., floral structural studies on suprafamilial clades of 1993; Soltis, Gitzendanner & Soltis, 2007; Zhu et al., rosids. Among angiosperms, rosids are an especially 2007; APG III, 2009; Wang et al., 2009; Christenhusz et al., 2010; Qiu et al., 2010). Most of these newly *Corresponding author. E-mail: [email protected] recognized clades still need to be characterized © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166, 331–416 331 332 M. L. MATTHEWS and P. K. ENDRESS structurally and biologically in order to gain inte- ceae) belonging instead to Cucurbitales (Schwarzbach grated knowledge of their properties and their evolu- & Ricklefs, 2000; Zhang et al., 2006). Anisophylleaceae tionary biology. However, this is a long-term goal as were sometimes also placed in other rosid orders such studies are time-consuming. First attempts have (Cronquist, 1981; Tobe & Raven, 1987a; Dahlgren, already been made focusing on the entire rosid clade 1988; Juncosa & Tomlinson, 1988a, b; discussion on (Endress & Friis, 2006; Endress & Matthews, 2006b; floral structure, Tobe & Raven, 1988a; Matthews et al., Schönenberger & von Balthazar, 2006; Endress, 2001). 2010a) and on specific orders or clusters of families The position of Rhizophoraceae with other families (Matthews et al., 2001; Matthews & Endress, 2002, now constituting Malpighiales (Erythroxylaceae not 2004, 2005a, b, 2006, 2008; Bachelier & Endress, included) was first identified in the molecular study 2008, 2009). Malpighiales, with 35 families listed in by Conti, Litt & Sytsma (1996) [Rhizophoraceae + Downloaded from https://academic.oup.com/botlinnean/article/166/4/331/2418590 by guest on 26 September 2021 APG III (2009), are the largest and most recalcitrant Drypetes Vahl sister to Humiriaceae + (Euphorbia clade of rosids in terms of phylogenetic resolution L. + Malpighiaceae)]. Earlier, Rhizophoraceae were (Davis, Xi & Wurdack, 2008a; Korotkova et al., 2009; commonly placed in or close to Myrtales or with Wurdack & Davis, 2009; Soltis et al., 2011). families that are now in Myrtales (Endlicher, 1836– It has been assumed that the difficulties in phylo- 1840, 1841; Bentham & Hooker, 1862–1867; Baillon, genetic resolution, especially in Malpighiales, are the 1876; Schimper, 1893; Dahlgren, 1983; Takhtajan, result of an explosive radiation in the mid-Cretaceous 1987) or with Cornales (Thorne, 1983). However, (Davis et al., 2005; Magallón & Castillo, 2009; Wang already Hallier (1921: 95) regarded Rhizophoraceae et al., 2009). The most surprising recent phylogenetic as related to Linaceae. According to Cronquist (1981) discovery is that the giant-flowered Rafflesiaceae are they were difficult to place, with Myrtales, Cornales members of Malpighiales and that they are closely or Rosales, or as a separate order, Rhizophorales (in related to Euphorbiaceae (Davis et al., 2007; Davis, Rosidae). Dahlgren (1988) assumed relationships of 2008; Davis, Endress & Baum, 2008b). Thus, floral Rhizophoraceae primarily with Elaeocarpaceae (now gigantism is a striking example of drastic evolution- in Oxalidales) and with Celastraceae (Celastrales), ary changes in the diversification of Malpighiales. but also discussed potential relationships with Eryth- The present study focuses on six families: Rhizopho- roxylaceae and some other groups, and Keating & raceae, Erythroxylaceae, Ctenolophonaceae, Linaceae, Randrianasolo (1988) found similarities with Hugonia Irvingiaceae and Caryocaraceae. These families have L. (Linaceae), among other groups. In contrast to been placed in very different orders in premolecular Rhizophoraceae, Erythroxylaceae were placed close to classifications. Some are known for single familiar other families of the current Malpighiales, such as genera, such as flax and linseed (Linum L., Linaceae), Malpighiaceae (de Jussieu, 1789; Endlicher, 1836– coca (Erythroxylum P.Browne, Erythroxylaceae) or 1840, 1841 and Linaceae (Bentham & Hooker, 1862– mangroves (Rhizophora L. and some other genera of 1867; Baillon, 1873, 1874; Gundersen, 1950; Rhizophoraceae). Of the six families, only the sister Oltmann, 1968) or Linales–Rosidae (Cronquist, 1981). relationship of Rhizophoraceae and Erythroxylaceae is With regard to the other four families considered currently most robustly supported. It was first found here, Caryocaraceae + [Linaceae + Irvingiaceae] are (with moderate support) in an rbcL study by Setoguchi, sister to Rhizophoraceae + Erythroxylaceae in the Kosuge & Tobe (1999) and a study with atpB and rbcL angiosperm analysis by Soltis et al. (2007) with narrow by Savolainen et al. (2000a), but Schwarzbach & Rick- sampling within Malpighiales, but without strong lefs (2000) found strong support for this sister clade support (Fig. 1A), whereas Ctenolophonaceae appear based on plastid DNA and nuclear DNA analyses, and as sister to Rhizophoraceae + Erythroxylaceae in the this relationship was clearly confirmed by further large 13-loci analysis of Malpighiales by Wurdack & studies (Tokuoka & Tobe, 2006; Korotkova et al., 2009; Davis (2009) (Fig. 1B), also without strong support, Wurdack & Davis, 2009; Soltis et al., 2011). That Ery- and similarly in the recent 17-loci, 640-taxon throxylaceae are related to Rhizophoraceae was first angiosperm-wide analysis of Soltis et al. (2011). The assumed based on the shared special type of sieve-tube relationship between Caryocaraceae, Linaceae, and plastids (Behnke, 1982, 1988). Curiously, when the Irvingiaceae also lacks strong support (Soltis et al., genus Peglera Bolus (now in Nectaropetalum Engl. in 2007), and their positions are scattered in Malpighi- Erythroxylaceae) was first described by Bolus (1907), it ales in Wurdack & Davis (2009) and Soltis et al. (2011). was thought to be closely related to Rhizophoraceae Linaceae and some related families
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