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Patterns and development of floral asymmetry in Senna (Leguminosae, Cassiinae)

Authors:
  • Natural History Museum of Canton Ticino, Lugano, Switzerland

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The buzz-pollinated genus Senna (Leguminosae) is outstanding for including species with monosymmetric flowers and species with diverse asymmetric, enantiomorphic (enantiostylous) flowers. To recognize patterns of homology, we dissected the floral symmetry character complex and explored corolla morphology in 60 Senna species and studied floral development of four enantiomorphic species. The asymmetry morph of a flower is correlated with the direction of spiral calyx aestivation. We recognized five patterns of floral asymmetry, resulting from different combinations of six structural elements: deflection of the carpel, deflection of the median abaxial stamen, deflection or modification in size of one lateral abaxial stamen, and modification in shape and size of one or both lower petals. Prominent corolla asymmetry begins in the earl-stage bud (unequal development of lower petals). Androecium asymmetry begins either in the midstage bud (unequal development of thecae in median abaxial stamen; twisting of androecium) or at anthesis (stamen deflection). Gynoecium asymmetry begins in early bud (primordium off the median plane, ventral slit laterally oriented) or midstage to late bud (carpel deflection). In enantiostylous flowers, pronouncedly concave and robust petals of both monosymmetric and asymmetric corollas likely function to ricochet and direct pollen flow during buzz pollination. Occurrence of particular combinations of structural elements of floral symmetry in the subclades is shown.
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... Although pollen and stigma are commonly leveled within a typical flower, this is not the case in many Senna flowers: the pistil can be twice as long as the stamens (Figure 22.1c). In most sennas, the pistil is deflected to the left or to the right from the middle plane of the flower (enantiostyly; Figure 22.1c) (Marazzi and Endress, 2008). As a consequence of a long, deflected pistil, the stigma touches the pollinating bees on their dorsal side (thorax or abdomen, depending on the Senna species), while the short stamens are all on the ventral side of the bee (Westerkamp, 2004;Amorim et al., 2017). ...
... Marazzi et al. (2006) proposed seven major clades for genus Senna. A description of floral architecture of Senna flowers is available in the studies by Marazzi et al. (2007) and Marazzi and Endress (2008), and is summarized in Figure 22.3. Species of clade I retain the ancestral traits of flower morphology, showing monosymmetric (zygomorphic) flowers similar to those of genus Cassia, the sister group of Senna (Marazzi et al., 2006). ...
... Species of clade I retain the ancestral traits of flower morphology, showing monosymmetric (zygomorphic) flowers similar to those of genus Cassia, the sister group of Senna (Marazzi et al., 2006). Monosymmetric flowers are also found in the most derived clade VII, but it is likely a case of reversal (Marazzi et al., 2006(Marazzi et al., , 2007(Marazzi et al., , 2008. Asymmetric (enantiomorphic) flowers are found mostly between clades II and VI. ...
... When the petal was positioned to the right of the floral axis, the flower was considered left-styled, and when it was positioned to the left, the flower was considered right-styled ( Fig. 1; Almeida et al., 2013b). The use of the curved petal to classify the floral type is common in studies with enantiostylous Cassiinae species, as its position opposite to the insertion point of the style is a consistent pattern in the group (Westerkamp, 2004;Marazzi and Endress, 2008;Almeida et al., 2013a, 2013b, Almeida et al., 2015a, 2015bAmorim et al., 2017). To test whether the ratios between right-and left-styled flowers were balanced within the individuals studied (~0.5 ratios: isoplethy), a generalized linear mixed-effect model (GLMM) was performed using the glm function in the lme4 package in R (Bates et al., 2018). ...
Article
Differences in the arrangement of floral whorls in enantiostylous species may affect the levels of reciprocity between the sexual organs of floral morphs and the functionality of the enantiostyly. In this study, we aimed to investigate enantiostyly in Senna rugosa, evaluating the variation in the position of sexual organs. Using different spatial measures, we investigated the level of herkogamy and used the inaccuracy index to describe the level of reciprocity between stigmas and anthers of different floral types and within the same floral type. We investigated the proportion of floral types within individuals of the population based on the position of the curved petal and the stigma. Stigmas of left-styled flowers are more likely to capture inter-morph pollen, whereas stigmas of right-styled flowers may receive greater proportions of intra-morph pollen. Horizontal distance was most responsible for the non-overlap of the sexual organs, whereas height was the measure that contributed most to their proximity. Individuals showed a similar proportion of floral types. However, from a morpho-functional perspective, the proportion of flowers differed, with a lower proportion of functionally left-styled flowers. Both floral types have functionally right-, left-, and central-styled flowers. Our study is the first report of a possible division of reproductive functions in pollen uptake between opposite floral types, a mechanism that may have evolved to provide reproductive assurance, and the second report of the presence of functionally central styles within the subtribe Cassiinae, which may be related to an increase in the pollen-capturing surface area on the pollinator body.
... In actinomorphic flowers the staminodes replace the staminal whorl and this is an irreversible process whereas in zygomorphic flowers the staminodes are present in different whorls as subset and they once lost can reappear in a lineage as in case of Senna. Sometimes staminodes acquire new functions and are lost quickly whereas the nonfunctional staminodes are considered as advanced character appeared only in recently derived taxa (Walker-Larsen and Harder, 2000;Marazzi and Endress, 2008). ...
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Taxonomically and phylogenetically Senna species complex is quite intriguing having several status and origin related issues. Keeping this view in mind and scope of cytological investigation 10 species of same genus viz. S. alata, S. alexandrina, S. italica, S. obtusifolia, S. occidentalis, S. polyphylla, S. siamea, S. sulfurea, S. surattensis and S. tora were analysed in cytological frame and comprehensive data/ information, is generated. The basic chromosomal analysis revealed regular meiotic behavior despite the occurrence of some irregularities. The regular occurrence of multivalents especially quadrivalents at diplotene as well as diakinesis stage and unavailability of individual having x=7 chromosome number possibly indicates paleopolyploid origin of worked out taxa. Individual anther basis pollen analysis provides some clues regarding on going evolutionary processes in the same genus. Considered cytological parameters based cluster analysis and their comparison with molecular marker based phylogenetic analysis of earlier workers revealed the efficacy of used parameters in phylogenetic characterization of Senna species complex.
... Those other metrics were similarly high between S. racemosa and P. mayanus; even so, C. dodecandra is likely the most important core plant species in our network because it had the highest nectar volume (Table 3), and C. dodecandra has been reported to be visited by C. canivetii in other Yucatan sites (Santamaria in Canch e-Coll ı & Canto, 2014). On the other hand, although S. racemosa is adapted to buzz pollination by bees (Marazzi et al., 2007;Marazzi & Endress, 2008), we did observe hummingbirds visiting it in our study site, and it had nearly the same nectar volume as C. dodecandra (Table 3). The mistletoe P. mayanus flowered more frequently than the other plants (Table 2) and it belongs to a family where all plants are dependent on animal pollinators (Vidal-Russell & Nickrent, 2008), but we did not find literature reports of this species' pollinators. ...
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Pollination by animals contributes to the production of nearly 87.5% of the seeds and fruits in the world. Hummingbirds are one of the main groups of pollinating birds in the Americas, and they form pollination networks with the plants they visit. Few hummingbird-plant networks have been studied in tropical dry forest, which is one of the vegetation types most affected by deforestation worldwide. In this study, we describe the characteristics of the core species of a mutualistic hummingbird-plant network in a lowland dry forest located on the Yucatan Peninsula of Mexico. The study lasted a full year, from August 2017 to June 2018. Using point counts and focal observations, we identified three species of hummingbirds that visited eight plant species. The network was highly connected and had three modules-one for each hummingbird species. The core hummingbird species was Chlorostilbon canivetii, and the key plants were Cordia dodecandra, Senna racemosa and Psittacanthus mayanus. This hummingbird-plant network is apparently driven by water availability, which determines plant phenology, which in turn, determines hummingbird activity. In the context of global extinction, the conservation of core species will be critical to maintain the interactions that support all of the species in the network.
... Although the term floral symmetry refers to the entire structure with all its constitutive parts (sepals, petals, androecium, and gynoecium), the descriptions apply primarily to the perianth (particularly the corolla) (Fambrini and Pugliesi, 2016). Plant corollas display extremely high variation in size, color, structure, and function, which are in continuous remodeling to adapt to different environmental conditions and pollinators (Ma et al., 2017), thus the important foundations for corolla symmetry is constantly changing (Marazzi and Endress, 2008;Lazaro and Totland, 2014;Moyroud and Glover, 2017;De Craene, 2018). Most plants morphological studies on corolla symmetry have been restricted to the perspective of planar projection are qualitative descriptions of its evolutionary trends: radial symmetry to bilateral symmetry, and then to asymmetry, based on the number of symmetry axes (Citerne et al., 2010). ...
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... In the genus Senna, it is common to find species with different number, shape and fertility of their stamens (heteranthery), and often this is accompanied by a not central gynoecium, but displaced off the flower centre (Tucker 1996;Marazzi et al. 2007;Marazzi & Endress 2008;Zhonglai et al. 2016). This latter characteristic in Senna could be accompanied by corolla asymmetry, which is expressed by different lengths among the five petals, where the adaxial petal is enlarged, and the abaxial ones curved to contained large stamens, and a displaced style. ...
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Senna acatlanensis is described and illustrated here. This species is restricted to a forest ecotone in southern Puebla (Mexico), and stands out by its unique large asymmetric flowers, with yellow petals that do not fade away to reddish-brown as they dry-out, heteromorphic and variable androecium; with four staminodes, ten or less fertile stamens; by its pendulous, cylindrical fruits, with chartaceous strigillose valves, and inter-seminal septa with a black-pulpy endocarp that surrounds exareolate seeds. These morphological attributes in addition to leaves with two pairs of leaflets, anthers with beaks, gynoecium multi-ovulated, and transversely oriented seed, turned broadside to the septa placed this new species within the series Bacillares. Illustrations, taxonomic comments, distribution and conservation status are provided with a key to the Mexican species of series Bacillares.
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Pollination syndromes describe recurring adaptation to selection imposed by distinct pollina-tors. We tested for pollination syndromes in Merianieae (Melastomataceae), which contain bee-(buzz-), hummingbird-, flowerpiercer-, passerine-, bat-and rodent-pollinated species. Further, we explored trait changes correlated with the repeated shifts away from buzz-pollination, which represents an 'adaptive plateau' in Melastomataceae. We used random forest analyses to identify key traits associated with the different pollinators of 19 Merianieae species and estimated the pollination syndromes of 42 more species. We employed morphospace analyses to compare the morphological diversity (disparity) among syndromes. We identified three pollination syndromes ('buzz-bee', 'mixed-vertebrate' and 'passerine'), characterized by different pollen expulsion mechanisms and reward types, but not by traditional syndrome characters. Further, we found that 'efficiency' rather than 'attraction' traits were important for syndrome circumscription. Contrary to syndrome theory, our study supports the pooling of different pollinators (hummingbirds, bats, rodents and flowerpiercers) into the 'mixed-vertebrate' syndrome, and we found that disparity was highest in the 'buzz-bee' syndrome. We conclude that the highly adaptive buzz-pollination system may have prevented shifts towards classical pollination syndromes, but provided the starting point for the evolution of a novel set of distinct syndromes, all having retained multifunctional stamens that provide pollen expulsion, reward and attraction.
... All other buzz-pollinated Merianieae have relatively large flowers with a polysymmetric perianth, but a distinctly monosymmetric androecium. Similar buzz-pollinated flowers are present in the genus Senna (Fabaceae, Marazzi & Endress, 2008;Amorim et al., 2017). Although Senna flowers are usually urceolate with pronounced heteranthery (Buchmann, 1983;Marazzi et al., 2007), this character combination is found only in buzz-bee group 2 (Fig. 3, flower 5). ...
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Pollination syndromes describe recurring adaptation to selection imposed by distinct pollinators. We tested for pollination syndromes in Merianieae (Melastomataceae), which contain bee‐ (buzz‐), hummingbird‐, flowerpiercer‐, passerine‐, bat‐ and rodent‐pollinated species. Further, we explored trait changes correlated with the repeated shifts away from buzz‐pollination, which represents an ‘adaptive plateau’ in Melastomataceae. We used random forest analyses to identify key traits associated with the different pollinators of 19 Merianieae species and estimated the pollination syndromes of 42 more species. We employed morphospace analyses to compare the morphological diversity (disparity) among syndromes. We identified three pollination syndromes (‘buzz‐bee’, ‘mixed‐vertebrate’ and ‘passerine’), characterized by different pollen expulsion mechanisms and reward types, but not by traditional syndrome characters. Further, we found that ‘efficiency’ rather than ‘attraction’ traits were important for syndrome circumscription. Contrary to syndrome theory, our study supports the pooling of different pollinators (hummingbirds, bats, rodents and flowerpiercers) into the ‘mixed‐vertebrate’ syndrome, and we found that disparity was highest in the ‘buzz‐bee’ syndrome. We conclude that the highly adaptive buzz‐pollination system may have prevented shifts towards classical pollination syndromes, but provided the starting point for the evolution of a novel set of distinct syndromes, all having retained multifunctional stamens that provide pollen expulsion, reward and attraction.
... Senna pendula belongs to clade VII (sensu Marazzi et al. 2007), in which most of the representatives have monosymmetric flowers that possess upper and lower petals with similar shapes or have lower petals slightly longer and thinner than the upper ones (Marazzi & Endress 2008). In the latter, the pollen jet of the long stamens is directed to an elastic concave petal then it is again deflected from a second upper petal until the pollen grains are finally deposited on the bee's dorsum. ...
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