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PREMISE: Floral shape (relative arrangement and position of floral organs) is critical in mediating fit with pollinators and maximizing conspecific pollen transfer particularly in functionally specialized systems. To date, however, few studies have attempted to quantify flowers as the inherently three-dimensional (3D) structures they are and determine the effect of intraspecific shape variation on pollen transfer. We here addressed this research gap using a functionally specialized system, buzz pollination, in which bees extract pollen through vibrations, as a model. Our study species, Meriania hernandoi (Melastomataceae), undergoes a floral shape change from pseudocampanulate corollas with more actinomorphically arranged stamens (first day) to open corollas with a more zygomorphic androecium (second day) over anthesis, providing a natural experiment to test how variation in floral shape affects pollination performance. METHODS: In one population of M. hernandoi, we bagged 51 pre-anthetic flowers and exposed half of them to bee pollinators when they were in either stage of their shape transition. We then collected flowers, obtained 3D flower models through x-ray computed tomography for 3D geometric morphometric analyses, and counted the pollen grains remaining per stamen (male pollination performance) and stigmatic pollen loads (female pollination performance). RESULTS: Male pollination performance was significantly higher in open flowers with zygomorphic androecia than in pseudo-campanulate flowers. Female pollination performance did not differ among floral shapes. CONCLUSIONS: These results suggest that there is an "optimal" shape for male pollination performance, while the movement of bees around the flower when buzzing the spread-out stamens results in sufficient pollen deposition regardless of floral shape.
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Melastomataceae , Abelhas , Animais , Flores , Polinização , Pólen , Lacunas de EvidênciasRESUMO
Animal pollinators mediate gene flow among plant populations, but in contrast to well-studied topographic and (Pleistocene) environmental isolating barriers, their impact on population genetic differentiation remains largely unexplored. Comparing how these multifarious factors drive microevolutionary histories is, however, crucial for better resolving macroevolutionary patterns of plant diversification. Here we combined genomic analyses with landscape genetics and niche modelling across six related Neotropical plant species (424 individuals across 33 localities) differing in pollination strategy to test the hypothesis that highly mobile (vertebrate) pollinators more effectively link isolated localities than less mobile (bee) pollinators. We found consistently higher genetic differentiation (FST ) among localities of bee- than vertebrate-pollinated species with increasing geographical distance, topographic barriers and historical climatic instability. High admixture among montane populations further suggested relative climatic stability of Neotropical montane forests during the Pleistocene. Overall, our results indicate that pollinators may differentially impact the potential for allopatric speciation, thereby critically influencing diversification histories at macroevolutionary scales.
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Plantas , Polinização , Animais , Abelhas/genética , Biologia , Florestas , Geografia , Polinização/genética , VertebradosRESUMO
Evolutionary shifts from bee to vertebrate pollination are common in tropical mountains. Reduction in bee pollination efficiency under adverse montane weather conditions was proposed to drive these shifts. Although pollinator shifts are central to the evolution and diversification of angiosperms, we lack experimental evidence of the ecological processes underlying such shifts. Here, we combine phylogenetic and distributional data for 138 species of the Neotropical plant tribe Merianieae (Melastomataceae) with pollinator observations of 11 and field pollination experiments of six species to test whether the mountain environment may indeed drive such shifts. We demonstrate that shifts from bee to vertebrate pollination coincided with occurrence at high elevations. We show that vertebrates were highly efficient pollinators even under the harsh environmental conditions of tropical mountains, whereas bee pollination efficiency was lowered significantly through reductions in flower visitation rates. Furthermore, we show that pollinator shifts in Merianieae coincided with the final phases of the Andean uplift and were contingent on adaptive floral trait changes to alternative rewards and mechanisms facilitating pollen dispersal. Our results provide evidence that abiotic environmental conditions (i.e. mountain climate) may indeed reduce the efficiency of a plant clade's ancestral pollinator group and correlate with shifts to more efficient new pollinators.
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Flores , Polinização , Animais , Abelhas , Filogenia , Pólen , VertebradosRESUMO
Floral adaptation to a single most effective functional pollinator group leads to specialized pollination syndromes. However, adaptations allowing for pollination by two functional groups (bimodal pollination systems) remain a rarely investigated conundrum. We tested whether floral scent and nectar traits of species visited by two functional pollinator groups indicate specialization on either of the two pollinator groups or adaptations of both (bimodal systems). We studied pollination biology in four species of Meriania (Melastomataceae) in the Ecuadorian Andes. Pollinator observations and exclusion experiments showed that each species was effectively pollinated by two functional groups (hummingbirds/bats, hummingbirds/rodents, flowerpiercers/rodents), nectar composition followed known bird preferences, and scent profiles gave mixed support for specialization on bats and rodents. Our results suggest that nectar-rewarding Meriania species have evolved stable bimodal pollination strategies with parallel adaptations to two functional pollinator groups. The discovery of rodent pollination is particularly important given its rarity outside of South Africa.
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Adaptação Biológica , Melastomataceae , Néctar de Plantas , Polinização , Animais , Aves , Quirópteros , Odorantes , RoedoresRESUMO
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.
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Adaptação Fisiológica , Abelhas/fisiologia , Flores/fisiologia , Fenômenos Fisiológicos Vegetais , Plantas/genética , Animais , Evolução Biológica , Aves , Flores/genética , Polinização , VertebradosRESUMO
Heteranthery, the presence of distinct stamen types within a flower, is commonly explained as functional adaptation to alleviate the "pollen dilemma," defined as the dual and conflicting function of pollen as pollinator food resource and male reproductive agent. A single primary hypothesis, "division of labor," has been central in studies on heteranthery. This hypothesis postulates that one stamen type functions in rewarding pollen-collecting pollinators and the other in reproduction, thereby minimizing pollen loss. Only recently, alternative functions (i.e., staggered pollen release), were proposed, but comparative and experimental investigations are lagging behind. Here, we used 63 species of the tribe Merianieae (Melastomataceae) to demonstrate that, against theory, heteranthery occurs in flowers offering rewards other than pollen, such as staminal food bodies or nectar. Although shifts in reward type released species from the "pollen dilemma," heteranthery has evolved repeatedly de novo in food-body-rewarding, passerine-pollinated flowers. We used field investigations to show that foraging passerines discriminated between stamen types and removed large stamens more quickly than small stamens. Passerines removed small stamens on separate visits towards the end of flower anthesis. We propose that the staggered increase in nutritive content of small stamens functions to increase chances for outcross-pollen transfer.
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Polinização , Caracteres Sexuais , Flores , Pólen , ReproduçãoRESUMO
A new species collected in the lowland forests of the Chocó region of Ecuador, Sloanea cayapensis, is described and illustrated and its morphological similarities with other species of Sloanea are discussed.
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[This corrects the article DOI: 10.1038/s42003-019-0697-7.].
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Angiosperm flowers have diversified in adaptation to pollinators, but are also shaped by developmental and genetic histories. The relative importance of these factors in structuring floral diversity remains unknown. We assess the effects of development, function and evolutionary history by testing competing hypotheses on floral modularity and shape evolution in Merianieae (Melastomataceae). Merianieae are characterized by different pollinator selection regimes and a developmental constraint: tubular anthers adapted to specialized buzz-pollination. Our analyses of tomography-based 3-dimensional flower models show that pollinators selected for functional modules across developmental units and that patterns of floral modularity changed during pollinator shifts. Further, we show that modularity was crucial for Merianieae to overcome the constraint of their tubular anthers through increased rates of evolution in other flower parts. We conclude that modularity may be key to the adaptive success of functionally specialized pollination systems by making flowers flexible (evolvable) for adaptation to changing selection regimes.
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We compiled a data set for all tree species collected to date in lowland Amazonian Ecuador in order to determine the number of tree species in the region. This data set has been extensively verified by taxonomists and is the most comprehensive attempt to evaluate the tree diversity in one of the richest species regions of the Amazon. We used four main sources of data: mounted specimens deposited in Ecuadorian herbaria only, specimen records of a large-scale 1-hectare-plot network (60 plots in total), data from the Missouri Botanical Garden Tropicos® database (MO), and literature sources. The list of 2,296 tree species names we provide in this data set is based on 47,486 herbarium records deposited in the following herbaria: Alfredo Paredes Herbarium (QAP), Catholic University Herbarium (QCA), Herbario Nacional del Ecuador (QCNE), Missouri Botanical Garden (MO), and records from an extensive sampling of 29,768 individuals with diameter at breast height (dbh) ≥10 cm recorded in our plot network. We also provide data for the relative abundance of species, geographic coordinates of specimens deposited in major herbaria around the world, whether the species is native or endemic, current hypothesis of geographic distribution, representative collections, and IUCN threat category for every species recorded to date in Amazonian Ecuador. These data are described in Metadata S1 and can be used for macroecological, evolutionary, or taxonomic studies. There are no copyright restrictions; data are freely available for noncommercial scientific use (CC BY 3.0). Please see Metadata S1 (Class III, Section B.1: Proprietary restrictions) for additional information on usage.