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The Immense Diversity of Floral Monosymmetry and Asymmetry Across Angiosperms
Abstract
Floral monosymmetry and asymmetry are traced through the angiosperm orders and families. Both are diverse and widespread in angiosperms. The systematic distribution of the different forms of monosymmetry and asymmetry indicates that both evolved numerous times. Elaborate forms occur in highly synorganized flowers. Less elaborate forms occur by curvature of organs and by simplicity with minimal organ numbers. Elaborate forms of asymmetry evolved from elaborate monosymmetry. Less elaborate form come about by curvature or torsion of organs, by imbricate aestivation of perianth organs, or also by simplicity. Floral monosymmetry appears to be a key innovation in some groups (e.g., Orchidaceae, Fabaceae, Lamiales), but not in others. Floral asymmetry appears as a key innovation in Phaseoleae (Fabaceae). Simple patterns of monosymmetry appear easily “reverted” to polysymmetry, whereas elaborate monosymmetry is difficult to lose without disruption of floral function (e.g., Orchidaceae). Monosymmetry and asymmetry can be expressed at different stages of floral (and fruit) development and may be transient in some taxa. The two symmetries are most common in bee-pollinated flowers, and appear to be especially prone to develop in some specialized biological situations: monosymmetry, e.g., with buzz-pollinated flowers or with oil flowers, and asymmetry also with buzz-pollinated flowers, both based on the particular collection mechanisms by the pollinating bees. Floral monosymmetry has developed into a model trait in evo-devo studies, whereas floral asymmetry to date has not been tackled in molecular genetic studies.
... Zygomorphy (or monosymmetry) is one of mani fes tations of symmetry in flowers and one of the most promi nent homoplastic traits in angiosperms (Endress 1999, 2001, 2012, Rudall & Bateman 2004, Jabbour et al. 2009, Ci ter ne et al. 2010, Reyes et al. 2016, Bukhari et al. 2017. Zygo morphic flowers have only one symmetry plane and thus show a bilateral symmetry along so-called plane of zygomorphy. ...
... Zygo morphic flowers have only one symmetry plane and thus show a bilateral symmetry along so-called plane of zygomorphy. Zygomorphy can be classified into two types -positional and constutional (Endress 1999(Endress , 2012. The positional zygomorphy is mainly led by gravity and occurs in taxa with predominantly polysymmetric flowers. ...
... The flowers are conspicuously monosym metric with clear differences between the upper (dorsal) and lower (ventral) sides (Bukhari et al. 2017). The stamens and the pistil are often hidden in the keel on the lower side of in the lip on the upper side (Endress 1994, 2012, Westerkamp & Claßen-Bockhoff 2007. Zygomorphy by reduction or simplicity as well as the elaborate zygomorphy represents a structural type. ...
Pendent sessile flowers of Chamaelirium japonicum (Willd.) N. Tanaka appear zygomorpic, but they do not possess a bilateral symmetry. The flowers are subtended by a vestigial bract and lack a bracteole. The perianth consists of two small tepals on the abaxial side of the flower and four large tepals, none of which is median. Because the short tepals belong to different whorls, there is no symmetry plane. Despite the absence of a bracteole, the shape of the floral meristem before peri anth inception resembles that of bracteolate monocot flowers. At early stages, all six tepals are equal in shape and size, and the flower is actinomorphic. The differ ence between the dorsal and ventral sides and the pendent nature of the flower become expressed during the gynoecium development. The absence of median organs allows to avoid collision of floral organs with the flower-subtending bract during flower curvature. Species of Chamaelirium reveal a set of different flower groundplans, which makes the genus a perfect model to investigate evolutionary changes in flower symmetry accompanied by differential tepal reduction.
... In angiosperms, zygomorphic (monosymmetric) flowers have been independently derived several times from actinomorphic (polysymmetric) flowers. The feature is dominating in large families like Lamiaceae and Scrophulariaceae (Endress 1999(Endress , 2012. The evolutionary pathways of the floral symmetry in Lamiaceae have been studied by mapping them on phylogenetic trees. ...
... Monosymmetry is expressed at different organs (Endress 1999(Endress , 2012 and different stages of floral ontogeny from calyx inception until stamen initiation (Payer 1857, Lang 1906, Jiang and Moubaydin 2022. In Lamiaceae, three types of monosymmetry are found including very early, early and late monosymmetry. ...
Since the first description of Salvia majdae (syn. Zhumeria majdae ) in 1967, its taxonomic status has remained an enigma within Salvia senso lato due to its unusual characters, in particular the floral structure. Based on recent molecular phylogenetic data, two defensible opinions on its status have been proposed. Here, we studied the floral development of this species using scanning electron microscopy to resolve this ambiguity. The aspects of floral symmetry were also studied. Like species of Salvia and representative genera of Lamiaceae, the initiation sequence of sepals and stamens in S. majdae is unidirectional from adaxial to abaxial and reverse, respectively. The flowers show temporal overlaps in initiation of petals and stamens. However, in contrast, the bidirectional initiation of the petals in S. majdae is reversed, starting with the abaxial middle petal, followed by the two adaxial ones, and then finally ending with the two lateral ones. The filaments of the sterile stamens are elongated and exposed as staminodes thorough development. We conclude that subequal growth of the calyx lips, weak cochlear aestivation and bidirectional initiation of the petals and well‐developed sterile stamen primordia are responsible for the weak floral asymmetry in S. majdae . Based on these data, S. majdae shows significant differences from Salvia .
... In zygomorphic (monosymmetric) and asymmetric flowers found throughout the angiosperms, floral symmetry patterns are often the results of the elaboration and/or abortion of distinct floral organs [3,4]. The asymmetry of Canna flowers is primarily due to the irregular petaloidy among the androecial members, a fertile stamen, and several staminodes, which dominate the floral display. ...
... The asymmetric flower is correlated with the asymmetric surroundings in which it developed, as seen with the lateral cincinnus of Canna. A similar phenomenon was observed in Tradescantia (Commelinaceae), the flower of which is arranged in a monochasial partial florescence and has a transient slight asymmetry in its early developmental stages [3]. ...
Floral symmetry studies often focus on the development of monosymmetric and polysymmetric flowers, whereas asymmetric flowers and their position and function within the inflorescence structure are largely neglected. Cannaceae is one of the few families that possesses truly asymmetric flowers, serving as a model to study the characters and mechanisms involved in the development of floral asymmetry and its context within the developing and mature inflorescence. In this study, inflorescence structure and floral morphology of normal asymmetric flowers and 16 aberrant flower collections from Canna indica L. and C. glauca L. were photographed, analyzed, and compared with attention to stamen petaloidy, floral symmetry, and inflorescence branching patterns anterior and posterior to the aberrant flower. In comparison with normal flowers, the aberrant flowers are arranged into abnormal partial florescences, and vary in floral symmetry, orientation, and degree of androecial petaloidy. The appendage of the fertile stamen is universally located distal from the higher order bract, indicating an underlying influence of inflorescence architecture. A synthetic model is proposed to explain the relationship between floral symmetry and inflorescence structure. Data from the observation of aberrant phenotypes strongly support the hypothesis that irregular petaloidy of the stamens is correlated with an asymmetric morphogenetic field within the inflorescence that contributes to the overall floral asymmetry in Canna flowers.
... Depending on the extent and time of bract pressure, the floral apex retains its original form or expands with further organ initiation. This change is associated with transitions in symmetry during development which occurs in many clades (see Endress 2012;Tucker 1999). Bracts may also exercise pressure on the flower in the form of an epicalyx. ...
Heterochrony acts as a fundamental process affecting the early development of organisms in creating a subtle shift in the timing of initiation or the duration of a developmental process. In flowers this process is linked with mechanical forces that cause changes in the interaction of neighbouring floral organs by altering the timing and rate of initiation of organs. Heterochrony leads to a delay or acceleration of the development of neighbouring primordia, inducing a change in the morphospace of the flowers. As changes in the timing of development may affect organs differently at different stages of development, these shifts eventually lead to major morphological changes such as altered organ positions, fusions, or organ reductions with profound consequences for floral evolution and the diversification of flowers. By concentrating on early developmental stages in flowers it is possible to understand how heterochrony is responsible for shifts in organ position and the establishment of a novel floral Bauplan. However, it remains difficult to separate heterochrony as a process from pattern, as both are intimately linked. Therefore it is essential to connect different patterns in flowers through the process of developmental change.
Examples illustrating the importance of heterochronic shifts affecting different organs of the flower are presented and discussed. These cover the transition from inflorescence to flower through the interaction of bracts and bracteoles, the pressure exercised by the perianth on the androecium and gynoecium, the inversed influence of stamens on petals, and the centrifugal influence of carpels on the androecium. Different processes are explored, including the occurrence of obdiplostemony, the onset of common primordia, variable carpel positions, and organ reduction and loss.
... Consistent pollen placement and pick up in buzz pollinated flowers can be facilitated by bilaterally symmetric flowers (or asymmetric ones in the case of enantiostylous flowers with reciprocally deflected anthers and style), which can induce pollinators to alight in a consistent position among visits, potentially also increasing the accuracy of pollen transfer (Endress, 1999, Armbruster, 2022, Nevard and Vallejo-Marín, 2022. Monosymmetry and asymmetry commonly evolve in buzz pollinated flowers (Endress, 2012). In fact, the evolution of heteranthery, where different sets of anthers within the same flower specialise on feeding and pollinating functions, relies on relatively accurate and consistent pollen placement on the body of the pollinator (Luo et al., 2008, Vallejo-Marin et al., 2009, Saab et al., 2021. ...
Buzz pollination, a type of interaction in which bees use vibrations to extract pollen from certain kinds of flowers, captures a close relationship between thousands of bee and plant species. In the last 120 years, studies of buzz pollination have contributed to our understanding of the natural history of buzz pollination, and basic properties of the vibrations produced by bees and applied to flowers in model systems. Yet, much remains to be done to establish its adaptive significance and the ecological and evolutionary dynamics of buzz pollination across diverse plant and bee systems. Here, we review for bees and plants the proximate (mechanism and ontogeny) and ultimate (adaptive significance and evolution) explanations for buzz pollination, focusing especially on integrating across these levels to synthesise and identify prominent gaps in our knowledge. Throughout, we highlight new technical and modelling approaches and the importance of considering morphology, biomechanics, and behaviour in shaping our understanding of the adaptive significance of buzz pollination. We end by discussing the ecological context of buzz pollination and how a multilevel perspective can contribute to explain the proximate and evolutionary reasons for this ancient bee-plant interaction.
... This large dataset also includes information on growth form (herbaceous vs. woody) and flower size (largest linear dimension) for practically all species, and on compatibility system (self-compatible vs. self-incompatible) for more than half of species. Even though flower symmetry may vary along a gradient (Endress, 2012), for the sake of simplicity each species was classified into one of two categories, actinomorphic and zygomorphic, based on photographs and species descriptions. This classification of flower symmetry took into consideration the frontal flower outline as determined by the sterile flower whorls (i.e., either the calyx or corolla). ...
Floral symmetry plays an important role in plant-pollinator interactions and may have remarkable impacts on angiosperm diversification. However, spatiotemporal patterns in floral symmetry and drivers of these patterns remain unknown. Here, using newly compiled floral symmetry (actinomorphy versus zygomorphy) data of 279,877 angiosperm species and their distributions and phylogenies, we estimated global geographic patterns and macroevolutionary dynamics of floral symmetry. We found that frequency of actinomorphic species increased with latitude, while that of zygomorphic species decreased. Solar radiation, present-day temperature, and Quaternary temperature change correlated with geographic variation in floral symmetry frequency. Evolutionary transitions from actinomorphy to zygomorphy dominated floral symmetry evolution, although the transition rate decreased with decreasing paleotemperature throughout the Cenozoic. Notably, we found that zygomorphy may not favor diversification of angiosperms as previously observed in some clades. Our study demonstrates the influence of (paleo)climate on spatiotemporal patterns in floral symmetry and challenges previous views about role of flower symmetry in angiosperm diversification.
Floral symmetry plays an important role in plant-pollinator interactions and may have remarkable impacts on angiosperm diversification. However, spatiotemporal patterns in floral symmetry and drivers of these patterns remain unknown. Here, using newly compiled floral symmetry (actinomorphy versus zygomorphy) data of 279,877 angiosperm species and their distributions and phylogenies, we estimated global geographic patterns and macroevolutionary dynamics of floral symmetry. We found that frequency of actinomorphic species increased with latitude, while that of zygomorphic species decreased. Solar radiation, present-day temperature, and Quaternary temperature change correlated with geographic variation in floral symmetry frequency. Evolutionary transitions from actinomorphy to zygomorphy dominated floral symmetry evolution, although the transition rate decreased with decreasing paleotemperature throughout the Cenozoic. Notably, we found that zygomorphy may not favor diversification of angiosperms as previously observed in some clades. Our study demonstrates the influence of (paleo)climate on spatiotemporal patterns in floral symmetry and challenges previous views about role of flower symmetry in angiosperm diversification.
Floral morphology is key for understanding floral evolution and plant identification. Floral diagrams are two-dimensional representations of flowers that replace extensive descriptions or elaborate drawings to convey information in a clear and unbiased way. Following the same outline as the first edition, this comprehensive guide includes updated and relevant literature, represents the latest phylogeny, and features 28 new diagrams. Diagrams are presented in the context of the most recent classifications, covering a variety of families and illustrating the floral diversity of major groups of plants. A strong didactic tool for observing and understanding floral structures, these diagrams are the obvious counterpart to any genetic study in flowering plants and to the discussion of major adaptations and evolutionary trends of flowers. This book is invaluable for researchers and students working on plant structure, development and systematics, as well as being an important resource for plant ecologists, evolutionary botanists and horticulturists.
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).
Mature wood of Lactoris, not previously available for study, reveals ten distinctive characters: vessels with simple perforation plates; vessels in pore multiples; vessel-to-axial parenchyma pits scalariform or transitional, vessel-to-vessel pits alternate; fiber-tracheids with vestigial pits; fiber-tracheids, vessels, and axial parenchyma storied; axial parenchyma vasicentric scanty; axial parenchyma either not subdivided or, if subdivided, with thin nonlignified walls between the cells (like the septa in septate fibers); rays wide and tall, little altered during ontogeny; ray cells upright; and ray cells taller adjacent to fascicular areas. All of these features occur in woods of Piper and other Piperaceae. The systematic position of Lactoris is therefore reassessed. Evidence available to date is consonant with placement of Lactoridaceae in Piperales, in which it would be more primitive than Piperaceae or Saururaceae. Features cited as evidence for alternative placements of Lactoridaceae are reviewed.
Zur Entwicklungsgeschichte monosymmetrischer Dicotylen-Blüten. - Vaduz : Cramer, 1977. - 90 S. - Zugl.: Bonn, Univ., Diss. - (Dissertationes Botanicae ; 38)
A homolog is a part of the phenotype that is homologous to equivalent parts in other species. A biological homology concept is expected to explain three properties of homologs: 1) the conservation of those features that are used to define a homolog, 2) the individualization of the homolog with regard to the rest of the body, and 3) the uniqueness of homologs, i.e., their specificity for monophyletic groups. The main obstacle to describing a mechanistic basis for homology is the variability of the developmental pathways of undoubtedly homologous characters. However, not all aspects of the developmental pathway are of equal importance. The only organizational features of the developmental system that matter are those that have been historically acquired and cause developmental constraints on the further evolutionary modification of the characters. Two main factors contribute to historically acquired developmental constraints: generative rules of pattern formation and ontogenetic networks. In particular, hierarchical and cyclical inductive networks have the required properties to explain homology. How common such networks are is an open empirical question. The development and variation of pectoral fin hooks in blenniid fishes is presented as a model for the study of a simple ontogenetic network.
Analysing a large number of different grass flowers, a hypothesis is proposed to explain the floral variation found in the family. It is postulated that the interaction of the palea with the floral apex generates an area of inhibition wich substantially affects the floral apex. Depending on the mode of action in the reduction process, together with an independent phenomenon which affects the gynoecial organization, four major evolutionary patterns are recognized. The form of grass flower which has been most successful appears to be the bi-lodiculate, tri-staminate and bi-stigmatic, with the stamens belonging to two different cycles – the frontal from the outer whorl and the two lateral from the inner whorl.
