19 results in Flowers on the Tree of Life
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6 - Centrifugal stamens in a modern phylogenetic context: was Corner right?
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Summary
Introduction
The widespread occurrence of centrifugal stamen formation in some members of the group that we now term eudicots (tricolpates) led the influential tropical botanist E. J. H. Corner to suggest that ‘so profound a disturbance in floral development as the reversal of the androecium’ (Corner, 1946, p. 435) must be of considerable phylogenetic significance. Has Corner’s prediction proved correct, when viewed in a modern phylogenetic context? One reason that this question remains relevant today is that there is a considerable shortage of useful morphological synapomorphies that are taxonomically applicable at deep nodes within angiosperms. Most major groupings above the family level are defined by molecular, rather than morphological, differences, making them difficult to teach to students or to recognize in the field. In angiosperm taxonomy, the majority of characters relating to the flower are traditionally employed primarily at the species and genus level, or at best the family level. For example, differences in the degree of fusion between floral organs, both within and between floral whorls (especially petals and stamens), are often used to delimit species and genera. With the exception of syncarpy, characters relating to floral organ fusion are mostly too homoplastic to be taxonomically applicable at deeper nodes in angiosperms.
The character state ‘centrifugal stamens’, as defined by Corner (1946) and others, represents one aspect of centrifugal organ growth. Centrifugal growth in flowers was first documented by early morphologists (Payer, 1857; Eichler, 1875, 1878) and has been reviewed by several authors (e.g. Leins, 1964; Sattler, 1972b; Tucker, 1972, 1984; Rudall, 2010). It represents a complex set of morphogenetic phenomena, rather than a single developmental process (Rudall, 2010). Consistent with the Tree of Life theme of this volume, this chapter explores the taxonomic significance of this feature in the context of recent angiosperm classifications based on molecular data (e.g. Angiosperm Phylogeny Group III, 2009).
2 - Spatial separation and developmental divergence of male and female reproductive units in gymnosperms, and their relevance to the origin of the angiosperm flower
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Introduction: aims and terminology
It is now generally accepted that angiosperms are monophyletic and are derived from a gymnospermous ancestor. It is also widely recognized that, among extant seed-plants, angiosperm reproductive units are typically bisexual (= bisporangiate, hermaphrodite) and are termed flowers, whereas putatively comparable units produced by the four groups of gymnosperms represented in the extant flora are typically unisexual, either functionally dioecious (cycads, Ginkgo, gnetaleans) or a more complex admixture of dioecious and monoecious taxa (conifers) (e.g. Tandre et al., 1995). Individual extant gymnosperms are either monoecious, bearing male and female units on separate axes of the same plant, or dioecious, each individual bearing units of only one gender (note: in this chapter, the terms ‘male’ and ‘female’ are used consistently as colloquial shorthand for the ovuliferous and (pre)polleniferous conditions, respectively). A positive correlation with dispersal mechanism is evident, monoecious extant gymnosperms typically producing dry, wind-dispersed seeds and dioecious gymnosperms bearing fleshy, often animal-dispersed seeds (cf. Givnish, 1980; Donoghue, 1989).
Further terminological clarifications are needed. Bateman et al. (2006, p. 3472) reviewed relevant definitions before defining a flower as ‘a determinate axis bearing megasporangia that are surrounded by microsporangia and are collectively subtended by at least one sterile laminar organ’. Accepting this controversial definition means that the angiosperm flower is not unique; comparable hermaphrodite structures occur in at least one other group of seed-plants, specifically a putatively highly derived clade within bennettites (Crane, 1988). Extending this logic, the term inflorescence could also be applied more widely, to encompass axial systems that bear multiple reproductive units of gymnosperms. However, we have chosen to use throughout this chapter the more phylogenetically neutral term ‘truss’ to describe any reproductive shoot, unbranched or branched (we recognize that this usage of ‘truss’ contradicts that employed in the telome theory of Zimmermann, 1952).
9 - Multiplications of floral organs in flowers: a case study in Conostegia (Melastomataceae, Myrtales)
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Summary
Introduction
The genus Conostegia (Miconieae, Melastomataceae) includes shrubs and trees distributed in the Caribbean, Mexico, Central America, N Andes and Brazil (Schnell, 1996). At present, Conostegia contains about 40 species (Schnell, 1996; Mabberley, 1997), although over 100 names have been applied to the genus in the past. However, the elevated number of species has been explained as a probable misinterpretation of the intraspecific variation that occurs in some species (Schnell, 1996).
The name Conostegia, which is derived from the Greek words κονοσ = cone and στεγοσ = roof, was chosen by D. Don (1823) for grouping species characterized by flowers having their sepals fused into a cone-shaped calyptra (Fig 9.1 A–D). Despite the fact that a calyptrate calyx is present in other genera of the Melastomataceae, such as Bellucia, Blakea, Centronia, Henriettea, Llewellynia, Miconia and Pternandra (Schnell, 1996; Penneys et al., 2010), the peculiar calyx of Conostegia has long been regarded as a useful character for segregating Conostegia from other non-calyptrate species of Melastomataceae (Don, 1823). Species of Conostegia are immediately recognizable by the character combination of terminal inflorescences, flowers often multistaminate, calyx clearly circumscissily dehiscent at anthesis, anthers isomorphic and unappendaged, ovary inferior and berry fruits (Almeda, 2008).
1 - Introduction: Establishing the state of the art – the role of morphology in plant systematics
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Outlook
Scientific biological research is dominated by genetics and molecular studies nowadays. This research is extremely important and has led to a tremendous advance in the fields of systematic botany and evolutionary developmental genetics. Nevertheless, from the start the molecular approach grew at the expense of more traditional approaches, such as morphology, embryology, palynology and cytology, and today molecular Barcoding and phylogenetic studies often appear to be the dominant, sometimes exclusive, research areas. Despite this, most systematists would agree that morphological and molecular data are complementary and should, when possible, be used together in phylogenetic and evolutionary investigations. A common approach used in systematics, combining the molecular and morphological methods, routinely maps unexplored morphological characters or putative synapomorphies on well-supported phylogenetic trees in order to study the evolution of these characters. There is an important problem with this approach, that morphological characters can be wrongly defined or are often unknown or superficially assessed. However, understanding the characters used for phylogenetic studies is crucial for understanding evolutionary processes in plants.
A general appreciation of floral morphology is also becoming difficult to grasp, with the disappearance of generalists, and this is not helped by the fact that there is little or no funding for any PhDs that are non-molecular. With the cutback of traditional botany in university education, lack of interest and funding from decision-making bodies, floral morphology is left increasingly aside. This is tragic, because it represents a loss of knowledge, which needs to be ‘rediscovered’ (as currently happens with the oblivion of obscure nineteenth century observations in even more obscure journals) and a non-appreciation of the value of morphology in contributing to solving the biodiversity crisis. Alas, morphology and general botany are increasingly scrapped from university curricula in the constricted atmosphere of ‘efficient’ research funding, with retiring experts not being replaced and with an increased specialization in botany on offer. Very few universities still have a morphology-based, integrative botany course. Recent developments such as genetic Barcoding are undoubtedly useful, but they remove interest and funding from other studies, such as those focusing on floral morphology.
3 - New flowers of Laurales from the Early Cretaceous (Early to Middle Albian) of eastern North America
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Summary
Introduction
The increasing number of fossil angiosperm reproductive structures described from Cretaceous strata (e.g. Friis et al., 2006) has provided a wealth of new data for understanding aspects of early flowering-plant evolution. In particular, flowers retrieved from many newly discovered mesofossil floras are often three-dimensionally preserved, which permits detailed morphological and systematic analyses. They have thereby provided information on the phylogenetic diversity and reproductive biology of Cretaceous angiosperms (e.g. Friis et al., 2006, 2010). However, an important feature of the angiosperm fossil record from the Cretaceous is that many fossils, particularly from the Early Cretaceous, cannot readily be accommodated in living taxa at the family or genus level, either because they are too poorly preserved to show the diagnostic features needed for secure systematic placement, or because they show a mosaic of features found in several living groups, indicating that they represent extinct lineages on internal branches of the angiosperm phylogenetic tree. The focus of this paper is on two early fossils of the second kind. While their relationships to extant Laurales are secure, they show features indicating that they fall outside the circumscription of extant families in the order.
Studies of relationships among living angiosperms based on analyses of DNA sequences support the recognition of the Laurales as a monophyletic group of seven extant families (Calycanthaceae, Siparunaceae, Gomortegaceae, Atherospermataceae, Hernandiaceae, Monimiaceae, Lauraceae; Renner, 1999, 2005; Renner and Chanderbali, 2000). The Laurales are the sister group to Magnoliales and include between 2840 and 3340 species in about 92 genera (Renner, 2005). The Calycanthaceae are the well-supported sister group to the remainder of the order, the core Laurales (Fig 3.1), within which Atherospermataceae, Gomortegaceae and Siparunaceae also form a well-supported clade (e.g. Renner, 1999, 2005). Relationships among Lauraceae, Monimiaceae and Hernandiaceae are currently not settled securely (Renner and Chanderbali, 2000). Morphological data strongly support a sister relationship of Hernandiaceae and Lauraceae (e.g. Doyle and Endress, 2000; Endress and Doyle, 2009), as do some molecular analyses (e.g. Qiu et al., 1999, 2006). However, in other molecular analyses the pattern of relationships among these three families is not well resolved (e.g. Renner, 1999, 2005; Chanderbali et al., 2001; Soltis et al., 2007).
12 - Floral development of Napoleonaea (Lecythidaceae), a deceptively complex flower
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Introduction
Napoleonaea is a small genus with about eight to ten species mainly restricted to west and central Africa and extending into southern Africa (Liben, 1971; Frame and Durou, 2001). The genus was initially described by Palisot de Beauvois in 1804 and dedicated to Napoleon Buonaparte (Thompson, 1922; Liben, 1971), but became often misspelled as Napoleona in later publications.
Thompson (1922) reviewed the early classification of the genus. A close relationship with Myrtaceae was put forward by Bentham and Hooker (1867) on the belief that the corona of Napoleonaea represents sterile outer stamens, as found in some Myrtaceae and in the genera now placed in Lecythidaceae (e.g. Grias, Couroupita, Lecythis). The interpretation of the corolla is central in the discussion of affinities, as most authors accepted a Myrtalean affinity of Napoleonaea and Lecythidaceae (e.g. Masters, 1869; Baillon, 1875; Thompson, 1922, 1927). Later authors removed Lecythidaceae from Myrtales because of important morphological distinctions (see Dahlgren and Thorne, 1984). Recent molecular phylogenies have placed Lecythidaceae (including Napoleonaea) in Ericales (e.g. Morton et al., 1997; Schönenberger et al., 2005; APG, 2009).
5 - Changing views of flower evolution and new questions
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Flowers in phylogenetic and evolutionary studies
The role of flowers in evolutionary biology has changed in the past 20 years, as the major foci are constantly changing with new approaches and better understanding of evolutionary processes. The revolution of molecular phylogenetics and molecular developmental genetics produced a trend in flower studies away from phylogenetics and towards evolution. In turn, the discovery of many well-preserved Cretaceous fossil flowers led to a new trend in flower studies towards phylogenetics, because fossil flowers do not provide DNA. The following three current fields of flower structural studies may be distinguished:
Comparative morphological analysis of flowers – Many new major angiosperm clades have been recognized by molecular phylogenetic studies since Chase et al. (1993), as surveyed in APG (1998, 2009), Stevens (2001 onwards) and Soltis et al. (2005). These new clades need now to be critically studied comparatively in their structure and biology as they are largely unknown (e.g. Endress and Matthews, 2006; Endress, 2010a).
Morphology for phylogenetic studies – Flowers were generally used for phylogenetic studies in the era before the molecular revolution. In the past 20 years, phylogenetics has concentrated on molecular approaches, which yield more results in a shorter time than morphology. However, morphological phylogenetic analyses are still performed and yield interesting results, either alone or in combination with molecular analyses (at higher systematic levels, e.g. Nandi et al., 1998; Doyle and Endress, 2000, or lower levels, e.g. Carillo-Reyes et al., 2008; Sweeney, 2008). There has been a pessimistic attitude towards the use of morphological features in phylogenetics because of too much homoplasy (e.g. Givinish and Sytsma, 1997; Patterson and Givnish, 2002; Givnish, 2003; Scotland et al., 2003) and difficulties in scoring structural characters (Stevens, 2000). This is true if superficial structural features that are easy to spot are used (e.g. tepals large and showy versus small and inconspicuous, or fruits capsules versus berries, or storage organs rhizomes versus bulbs). However, morphology encompasses much more than such features. It can be expected that as our knowledge of flowers increases, there will be a resurgence in morphological phylogenetic analyses. In addition, the more fossil flowers become available, the more important morphological phylogenetic analyses will become (e.g. Friis et al., 2009; Doyle and Endress, 2010). There are not only many more fossil flowers available than 20 years ago, but there are also new techniques to reconstruct their morphology: the use of microtome section series (Schönenberger, 2005) and tomography (Friis et al., 2009). The search for and the detection of new structural patterns of interest is a continuing challenge. Characters and character states ‘cannot be defined but need to be discussed,’ as Wagner (2005) put it, meaning that definitions need to be constantly evaluated and updated to fit the current knowledge with each change in the phylogenetic framework. New knowledge on phylogeny (and evolution) continuously creates a new basis for discussion. Of course, if morphological characters are used for phylogenetic studies, this also means the necessity of repeated reciprocal illumination (see also Kelly and Stevenson, 2005). ‘Tree-thinking’ has been encouraged in evolutionary studies (O’Hara, 1988; Donoghue and Sanderson, 1992). This is of course also relevant for the focus on structural features, including the construction of morphological matrices for phylogenetic studies. The more detailed a tree under reconstruction already is and the more detailed our knowledge about the distribution of traits on this tree is, the better we can judge the quality of characters and character states to be scored.
Morphology for evolutionary studies – The new phylogenetic results can now be used to study the evolution of flowers on a much more solid basis than was possible before. A general result is that many features are more evolutionarily flexible than previously assumed. A number of examples are surveyed in this study. Rarely is a character more stable than previously assumed at macrosystematic level; such an exception are features of ovules (Endress, 2003, 2005a, 2010). However, such flexibility is not randomly distributed through the larger clades. Given features are more concentrated (but not universal) in a certain clade than in another one. Why is this so? Answers can be expected from better knowledge of the genetic systems that operate in the development of such features (e.g. Borowsky, 2008; Melzer et al., 2008). Thus, homoplasy in structure is pervasive, much more common than earlier imagined and is a fascinating aspect of flower evolution (e.g. Cantino, 1985; Endress, 1996). For more evolutionary aspects of flower morphology, see Endress (1994, 2003, 2005b, 2006).
Plate section
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Contents
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Frontmatter
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7 - Evolution of the palm androecium as revealed by character mapping on a supertree
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Summary
Introduction
Over the last two decades, our insight into the phylogenetic relationships among groups of living organisms has increased significantly (see, for example, the Tree of Life Project, Maddison et al., 2007). Since the first burst in phylogenetic analyses occurred in the early nineties triggered by the discovery of the PCR technique (Saiki et al., 1988), constant improvements in laboratory techniques have made it easier to reveal patterns of molecular variation across organisms (e.g. McCombie et al., 1992; Ronaghi, 2001). At the same time, computer power, access to online data and analytical tools have rapidly improved (see, for example, Guindon et al., 2003 and 2005). The most popular methods are based on most parsimonious reconstructions (MP) or Bayesian inference (BI), the latter allowing for molecular dating and therefore gaining in popularity (Huelsenbeck and Ronquist, 2001; Ronquist and Huelsenbeck, 2003). The methods have been implemented in user-friendly software such as MacClade (Maddison and Maddison, 2001), Bayestraits (available from http://www.evolution.rdg.ac.uk/BayesTraits.html, see also Pagel, 1999; Pagel et al., 2004) and the more recently developed Mesquite (Maddison and Maddison, 2009). As a consequence of these recent developments a large number of robust and highly resolved phylogenies are now available for various taxonomic levels, providing excellent frameworks for exploring character evolution through space and time.
The palms (Arecaceae or Palmae) are an iconic family of flowering plants comprising around 2400 species distributed worldwide. Palms constitute a highly distinctive component of tropical rain forests and often have major ecological impacts in the plant communities where they occur. At the same time they are of immense economic significance, both at the international level (e.g. oil palm, date palm, coconut, rattan) and at the village level, where they provide shelter and food. Research interest in the palm family has greatly increased in the last three decades. The results have recently been synthesized into a monograph, which describes the morphology, ecology and geographical distribution of all palm genera (Dransfield et al., 2008a). Several authors have contributed to unravelling the relationships among genera in the family (Asmussen and Chase, 2001; Hahn, 2002; Lewis and Doyle, 2002; Asmussen et al., 2006). The results have been summarized in a robust and comprehensive supertree phylogeny by Baker et al. (2009), including all genera of the family but the newly discovered Tahina (Dransfield et al., 2008b). This represents an excellent opportunity for studying evolutionary trends in morphological and ecological traits.
4 - Tracing the early evolutionary diversification of the angiosperm flower
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Summary
Introduction
The origin of the angiosperm flower and its subsequent evolution have been major topics of discussion and controversy for over a century. Because so many of the distinctive synapomorphies of angiosperms involve the flower, its origin and the homologies of its parts are closely tied to the vexed problem of the origin of angiosperms as a group. From a phylogenetic point of view, the origin of angiosperms involves two related problems: identification of the closest outgroups of angiosperms, which may clarify homologies of their distinctive features with structures seen in other plants, and rooting of the angiosperm phylogenetic tree and identification of its earliest branches, which may allow reconstruction of the flower in the most recent common ancestor of living angiosperms. It is this second topic that we address in this chapter (for the first study, see Frohlich and Chase, 2007; Doyle, 2008). This task has become much easier in the past ten years, thanks to molecular phylogenetics.
Ideas on the ancestral flower have varied greatly since early in the last century. Two extremes were euanthial theories, which postulated that the flower was a simple strobilus that was originally bisexual and had many free parts (Arber and Parkin, 1907), and pseudanthial theories, which assumed that the first angiosperms had unisexual flowers with few parts, as in ‘Amentiferae’ (now mostly Fagales), which were later grouped to form bisexual flowers (Wettstein, 1907; review in Friis and Endress, 1990). Later variations on the pseudanthial theory proposed that the angiosperms were polyphyletic (Meeuse, 1965, 1975), while recognition of chloranthoid pollen, leaves and flowers in the Early Cretaceous fossil record (Muller, 1981; Upchurch, 1984; Walker and Walker, 1984; Friis et al., 1986; Pedersen et al., 1991; Eklund et al., 2004) contributed to suggestions that Chloranthaceae, which combine putatively primitive wood and monosulcate pollen with extremely simple flowers, often consisting of just one stamen or one carpel, might provide another model for the ancestral flower (Endress, 1986b; Taylor and Hickey, 1992).
10 - Ontogenetic and phylogenetic diversification in Marantaceae
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Introduction
The Marantaceae Petersen (31 genera; ~530 ssp.: Andersson, 1998) are a pantropically (80% America; 11% Asia; 9% Africa: Kennedy, 2000) distributed family of perennial herbs and lianas found in the understory of tropical lowland rainforests. They are characterized by a unique pollination mechanism combining secondary pollen presentation with an explosive style movement (Kunze, 1984; Claßen-Bockhoff, 1991; Claßen-Bockhoff and Heller, 2008a). The specific pollen transfer mechanism is found in conjunction with a high synorganization of morphologically modified floral elements and has been postulated to be a key innovation responsible for the radiation of the Marantaceae (Kennedy, 2000).
Flowers in Marantaceae are trimerous, with inconspicuous sepals and petals and extremely modified elements in the two androeceal whorls (Fig 10.1). In the outer whorl one or two petaloid ‘outer staminodes’ act as the showy organs of the flowers. The three elements of the inner whorl are functionally differentiated into: (1) a single (monothecate) anther, (2) a ‘fleshy (callose) staminode’ and (3) a ‘hooded (cucullate) staminode’ (Kunze, 1984; Claßen-Bockhoff, 1991). These organs closely interact with the style resulting in secondary pollen presentation, set-up of tension and finally the explosive pollination mechanism (e.g. Gris, 1859; Delpino, 1869; Schumann, 1902; Yeo, 1993; Claßen-Bockhoff and Heller, 2008a, b; Ley, 2008; Pischtschan and Claßen-Bockhoff, 2008; Fig 10.2). As the style movement demands a high degree of synorganization of floral parts and synchronization with the pollinator and as the movement is irreversible, providing the flowers with a single opportunity for pollination, one should expect rather uniform structures across the whole family, as slight morphological deviations might result in a loss of operability. However, the high degree of floral diversity in the Marantaceae contradicts this expectation (Kunze, 1984; Kennedy, 2000; Claßen-Bockhoff and Heller, 2008a; Ley, 2008). It instead raises the questions: how far are elements of a functional unit allowed to vary without jeopardizing the reproductive success, and has the variation of the flowers influenced speciation in the family?
11 - Floral ontogeny of Acacia celastrifolia: an enigmatic mimosoid legume with pronounced polyandry and multiple carpels
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Introduction
The genus Acacia is among the largest plant genera. It was recently treated either in a broad sense with c. 1450 species (Lewis, 2005) or in a strict sense (Acacia s.s. with c. 987 species). The latter follows the re-typification of Acacia with an Australian type (Orchard and Maslin, 2003; see also Murphy, 2008). According to Maslin (1995), the Australian species A. celastrifolia belongs to the ‘Acacia myrtifolia group’ and is most closely related to A. myrtifolia. In molecular studies, only A. myrtifolia was sampled, which is sister to A. pulchella in the Pulchelloidea clade (e.g. Miller and Bayer, 2001; Miller et al., 2003; Murphy et al., 2010). Molecular sampling of the hitherto unsampled A. celastrifolia is highly desirable in order to verify the hypothesized close relationship with A. myrtifolia (e.g. Maslin, 1995).
Flowers of the genus Acacia s.l. are always found in globular heads or spikes. The flowers are (3–)4–5(–6)-merous, with free or united sepals and small reduced petals, which are postgenitally fused and which split open at anthesis. The androecium is composed of many free stamens (i.e. a polyandrous androecium) and the flower is normally terminated by a single superior carpel.
Acknowledgements
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Taxon index
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Subject index
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8 - Comparative floral structure and development of Nitrariaceae (Sapindales) and systematic implications
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Summary
Introduction
For the last 20 years, the development and improvement of molecular methods, based mostly on the comparison of DNA sequences, have been increasingly successful in reconstructing the phylogenetic tree of plants at all hierarchical levels. Consequently, they have contributed greatly to the recent improvement of angiosperm systematics. In addition, they have shown that earlier classifications, based mostly on plant vegetative and reproductive structures, had sometimes been misled by homoplastic characters, and a number of orders and families have had to be newly circumscribed or even newly established (e.g. APG, 1998, 2003, 2009; Stevens, 2001 onwards). These new results provide a novel basis for comparative structural studies to characterize the newly recognized clades and to evaluate clades that have only limited molecular support. However, because such comparative studies are time-consuming and the systematic classification has different hierarchical levels, they can only be done in a stepwise fashion (for eudicots, e.g. Matthews and Endress, 2002, 2004, 2005a, b, 2006, 2008; von Balthazar et al., 2004; Schönenberger and Grenhagen, 2005; Endress and Matthews, 2006; Ronse De Craene and Haston, 2006; von Balthazar et al., 2006; Bachelier and Endress, 2008, 2009; Janka et al., 2008; Schönenberger, 2009; von Balthazar and Schönenberger, 2009; Schönenberger et al., 2010).
As part of such a comparative approach, we studied the floral structure of Nitrariaceae, a small family which has been recently reclassified in Sapindales (APG, 2009). Nitrariaceae comprise four genera and around 15 species (Stevens, 2001 onwards; APG, 2009). They are native to arid and semi-arid regions of the Old World and are small to medium-sized shrubs (Nitraria; Engler, 1896a, b; Bobrov, 1965; Noble and Whalley, 1978), perennial herbs (Peganum and Malacocarpus; Engler, 1896a, 1931; El Hadidi, 1975) or small annual herbs of only a few centimetres height (Tetradiclis; Engler, 1896b, 1931; Hamzaoglu et al., 2005). In earlier classifications, the position and the mutual affinities of these genera varied tremendously, depending on the weight an author gave either to their vegetative or their reproductive features (Takhtajan, 1969, 1980, 1983, 2009; El Hadidi, 1975; Dahlgren, 1980; Cronquist, 1981, 1988; see Sheahan and Chase, 1996 for a detailed review of classifications). Because none of the traditional classifications was entirely satisfactory, however, most authors followed Engler’s influential work (1896a, b, 1931) and Nitraria, Tetradiclis and Peganum (including Malacocarpus) remained for a long time in their own subfamilies in Zygophyllaceae (Nitrarioideae, Tetradiclidoideae and Peganoideae; for more details of the history of classification, see Sheahan and Chase, 1996).
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