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Diverging Lineages in the Ericales Diversity and Evolution of Floral

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Diverging Lineages in the Ericales Diversity and Evolution of Floral Downloaded from rstb.royalsocietypublishing.org on January 4, 2010 Diversity and evolution of floral structure among early diverging lineages in the Ericales Jürg Schönenberger, Maria von Balthazar and Kenneth J. Sytsma Phil. Trans. R. Soc. B 2010 365, 437-448 doi: 10.1098/rstb.2009.0247 References This article cites 64 articles, 10 of which can be accessed free http://rstb.royalsocietypublishing.org/content/365/1539/437.full.html#ref-list-1 Rapid response Respond to this article http://rstb.royalsocietypublishing.org/letters/submit/royptb;365/1539/437 Subject collections Articles on similar topics can be found in the following collections taxonomy and systematics (194 articles) evolution (1308 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions This journal is © 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on January 4, 2010 Phil. Trans. R. Soc. B (2010) 365, 437–448 doi:10.1098/rstb.2009.0247 Diversity and evolution of floral structure among early diverging lineages in the Ericales Ju¨ rg Scho¨nenberger1,*,†, Maria von Balthazar2 and Kenneth J. Sytsma3 1Department of Botany, Stockholm University, Lilla Frescativa¨gen 5, 10691 Stockholm, Sweden 2Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, 10405 Stockholm, Sweden 3Department of Botany, University of Wisconsin, Madison, WI 53706-1831, USA This is a combination of review and original data on floral structure and diversity in the two earliest diverging lineages of the Ericales, i.e. the balsaminoids, comprising Balsaminaceae, Marcgraviaceae and Tetrameristaceae, and the polemonioids, comprising Fouquieriaceae and Polemoniaceae. Each clade is strongly supported in molecular studies, while structural synapomorphies have largely been lacking. For the balsaminoid families, we compare floral morphology, anatomy and histology among selected taxa and find that the entire clade is strongly supported by the shared presence of nectar- iferous tissue in the floral periphery, thread-like structures on anthers, truncate stigmas, secretion in the ovary, as well as mucilage cells, raphides and tannins in floral tissues. A possible sister group relationship between Balsaminaceae and Tetrameristaceae is supported by the shared presence of post-genital fusion of filaments and ovary and a star-shaped stylar canal. For polemonioids, we document unexpected diversity of floral features in Polemoniaceae, partly providing structural links to Fouquieriaceae. Features include cochlear and quincuncial corolla aestivation, connective protrusions, ventrifixed anthers and nectariferous tissue in the base of the ovary. In addition, we outline future directions for research on floral structure in the Ericales and briefly discuss the general importance of structural studies for our understanding of plant phylogeny and evolution. Keywords: asterids; Balsaminaceae; floral diversity; Marcgraviaceae; Polemoniaceae; Tetrameristaceae 1. INTRODUCTION (e.g. Cronquist 1981; Dahlgren 1983), many of which The stem node of the Ericales has been estimated to were thought to be distantly related (table 1). Only have its origin in the Mid-Early Cretaceous (Bremer the more recent rise of molecular phylogenetics made et al.2004), and the first major diversification, which possible our current understanding of the evolutionary gave rise to all major lineages of the order, probably history of the Ericales. Molecular studies have not took place 109–103 Myr ago (Sytsma et al.2006). By only demonstrated the monophyly of the order (Soltis the Early Eocene, i.e. ca 50 Myr ago, almost all extant et al. 2000; Albach et al.2001b), but also resolved the families had already diverged (Bremer et al.2004). Ericales as sister to the euasterids (figure 1; Bremer Today, Ericales comprise ca 6 per cent of the eudicot et al.2002). Within the order, families are generally species diversity (Magallo´n et al.1999) and include easily recognized based on morphological features and many well-known tropical as well as temperate groups. are mostly well supported in molecular studies. It has, In many tropical rainforests, they are an important however, proved difficult to disentangle interfamilial component of the understorey vegetation (ca 10% of relationships as most of the deeper nodes in the erica- the total species diversity; Davis et al.2005). They lean phylogeny remained unresolved or only weakly include ca 11 000 species in 347 genera and 25 families supported (Anderberg et al. 2002; Geuten et al. (Stevens 2001). In pre-molecular classification 2004). However, with the addition of more sequence systems, members of Ericales were usually assigned to data and a denser taxon sampling, subsequent studies between 10 and 12 different angiosperm orders have managed to improve resolution also at deeper levels in the ericalean tree (Scho¨nenberger et al. 2005; Sytsma et al. 2006). * Author for correspondence ([email protected]). † Present address: Department of Palynology and Structural Botany, Why were the Ericales not recognized as a natural Faculty Center of Biodiversity, University of Vienna, Rennweg 14, group in the pre-molecular era? Part of the answer 1030 Vienna, Austria. may lie in the considerable age of many of the families Electronic supplementary material is available at http://dx.doi.org/ and the corresponding long time spans of anagenic 10.1098/rstb.2009.0247 or via http://rstb.royalsocietypublishing.org. stem lineage evolution, which may have obscured One contribution of 16 to a Discussion Meeting Issue ‘Darwin and many structural synapomorphies. Today, members of the evolution of flowers’. the Ericales exhibit a vast diversity at all levels of 437 This journal is q 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on January 4, 2010 438 J. Scho¨nenberger et al. Ericales: floral diversity and evolution Table 1. Currently recognized families of Ericales (Stevens 2001; APG 2003) and pre-molecular, ordinal classifications remaining according to Cronquist (1981) and Dahlgren (1983). Ericales Subclass abbreviations: A, Asteridae; C, Corniflorae; D, Dilleniidae; M, Magnoliflorae; P, Primuliflorae; R, Rosidae; Ru, Rutiflorae; S, Solaniflorae; T, Theiflorae. Polemoniaceae ordinal classification of earlier Ericales Fouquieriaceae family names (no. authors of genera/species Marcgraviaceae according to Cronquist Stevens 2001) (1981) Dahlgren (1983) Tetrameristaceae Actinidiaceae Theales (D) Ericales (C) (3/355) Balsaminaceae Balsaminaceae Geraniales (R) Balsaminales asterids (2/1001) (Ru) euasterids Clethraceae (2/75) Ericales (D) Ericales (C) Cyrillaceae (2/2) Ericales (D) Ericales (C) Diapensiaceae Diapensiales (D) Ericales (C) Cornales (6/18) Figure 1. Phylogenetic relationships of Ericales and its two Ebenaceae (4/548) Ebenales (D) Ebenales (P) first diverging subclades; tree topology is based on Bremer Ericaceae Ericales (D) Ericales (C) et al. (2002), Scho¨nenberger et al. (2005) and Sytsma et al. (126/3395) (2006). Fouquieriaceae Violales (D) Fouquieriales (C) (1/11) Lecythidaceae Lecythidales (D) Theales (T) For instance, in his groundbreaking book The different (25/310) forms of flowers on plants and the same species (Darwin Maesaceae (1/150) Primulales (D) Primulales (P) Marcgraviaceae Theales (D) Theales (T) 1877), he collected a mass of data from morphological (7/130) observations and pollination experiments about Mitrastemonaceae Rafflesiales (R) Rafflesiales (M) phenomena such as heterostyly and cleistogamy. An (1/2) important part of his data is based on the study of eri- Myrsinaceae Primulales (D) Primulales (P) calean taxa including various representatives from (41/1435) Primulaceae, Polemoniaceae and Balsaminaceae. Pentaphylacaceae Theales (D) Theales (T) At present, there are no clear-cut non-molecular (14/340) synapomorphies neither for the order as a whole, nor Polemoniaceae Solanales (A) Solanales (S) for most of the major ericalean clades spanning more (18/385) than one family. The only feature shared by all taxa Primulaceae (9/900) Primulales (D) Primulales (P) is tenuinucellate ovules, but this is a characteristic of Roridulaceae (1/2) Rosales (R) Ericales (C) Sapotaceae Ebenales (D) Ebenales (P) most asterids (Albach et al. 2001a). One important (53/1100) reason for our inability to describe synapomorphies Sarraceniaceae Nepenthales (D) Sarraceniales (C) for larger clades within the Ericales, and, for that (3/15) matter, for many other large angiosperm clades, is Styracaceae Ebenales (D) Ebenales (P) that our current knowledge of the floral structure (11/160) and diversity of most families is highly fragmentary. Symplocaceae Ebenales (D) Cornales (C) In recent years, comparative structural analyses have (2/320) not kept pace with the ever faster evolving methods Tetrameristaceae Theales (D) Theales (T) for acquiring and analysing molecular sequence data, (3/5) and it is therefore currently difficult to test sequence- Theaceae (7/195) Theales (D) Theales (T) Theophrastaceae Primulales (D) Primulales (P) based phylogenetic hypothesis and to conduct (5/105) combined morphological/molecular analyses. This situation has been recognized as a fundamental pro- blem in angiosperm phylogenetics (Crane et al. their biology, including, for instance, mycorrhizal 2004), and the great need for new comparative struc- associations (e.g. Ericaceae p.p.), mycorrhizal
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