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Pollination syndromes. Bee-pollination syndrome: a)Dillwynia uncinata, showing the wing and keel that together act as a trigger mechanism. When a bee pushes down on the wings of a pea flower, the wings separate and trigger the sexual parts to rise out of the keel and deposit pollen from the anthers onto the bee. b) Flowers of Gastrolobium pyramidale. Bird-pollination syndrome: c)Leptosema aphyllum, showing the resupinate orientation and large size. d) Flowers of Gastrolobium rubrum. Figure a) adapted from Gross [16].

Pollination syndromes. Bee-pollination syndrome: a)Dillwynia uncinata, showing the wing and keel that together act as a trigger mechanism. When a bee pushes down on the wings of a pea flower, the wings separate and trigger the sexual parts to rise out of the keel and deposit pollen from the anthers onto the bee. b) Flowers of Gastrolobium pyramidale. Bird-pollination syndrome: c)Leptosema aphyllum, showing the resupinate orientation and large size. d) Flowers of Gastrolobium rubrum. Figure a) adapted from Gross [16].

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Interactions with pollinators are proposed to be one of the major drivers of diversity in angiosperms. Specialised interactions with pollinators can lead to specialised floral traits, which collectively are known as a pollination syndrome. While it is thought that specialisation to a pollinator can lead to either an increase in diversity or in some...

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... interactions are specialized, the plant typically exhibits a pollination syn- drome -a suite of floral characteristics that attract and provide food resources for a particular pollinator or pol- linator guild [12,13]. For example, a bird-pollination syn- drome typically involves large, red, tubular flowers, copious nectar and sexual parts positioned to deposit pollen on the bird (Figure 1). In contrast, bee-pollination syndromes have predominantly yellow, white or blue flowers (most hymenopteran pollinators have difficulty in discerning red flowers with a reflectance spectrum above 585 nm because they will not stand out from the green foliage [14,15]), a landing platform and guide marks and nutrient-rich nectar (Figure 1). ...
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... example, a bird-pollination syn- drome typically involves large, red, tubular flowers, copious nectar and sexual parts positioned to deposit pollen on the bird (Figure 1). In contrast, bee-pollination syndromes have predominantly yellow, white or blue flowers (most hymenopteran pollinators have difficulty in discerning red flowers with a reflectance spectrum above 585 nm because they will not stand out from the green foliage [14,15]), a landing platform and guide marks and nutrient-rich nectar (Figure 1). ...
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... legume tribes Mirbelieae and Bossiaeeae (the Australian "egg-and-bacon" peas) are a good system for addressing questions about floral transitions. Together, they comprise a diverse endemic Australian lineage in which species are specialised for either bee or bird pol- lination (Figure 1), as indicated both by direct observa- tion [22][23][24][25][26] and by morphological syndromes [27,28]. Here we use comparative analyses of dated molecular phylogenies to address two questions: ...
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... bee-pollination syndrome is clearly reconstructed as ancestral in the Australian egg-and-bacon peas ( Figures 3 and 4, Additional file 1: Figure S1 and Additional file 2: Figure S2). In all analyses, species with a bird-pollination syndrome are nested within clades of bee-pollinated taxa that are well supported by posterior probability (Bayesian) and bootstrap support (maximum likelihood) (Additional file 1: Figure S1 and Additional file 2: Figure S2). ...
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... bee-pollination syndrome is clearly reconstructed as ancestral in the Australian egg-and-bacon peas ( Figures 3 and 4, Additional file 1: Figure S1 and Additional file 2: Figure S2). In all analyses, species with a bird-pollination syndrome are nested within clades of bee-pollinated taxa that are well supported by posterior probability (Bayesian) and bootstrap support (maximum likelihood) (Additional file 1: Figure S1 and Additional file 2: Figure S2). The earliest transition to bird-pollination syndrome was reconstructed on the stem leading to the Leptosema clade. ...
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... relationships in the egg-and-bacon peas differed between estimates using cpDNA and ITS, resulting in slightly different reconstructions of transi- tions between bee-and bird-pollination syndromes (Additional file 1: Figure S1 and Additional file 2: Figure S2). This uncertainty in reconstructing shifts of pollinator syndrome is centred around relationships within Gastrolobium, many of which do not have strong support (Additional file 1: Figure S1 and Additional file 2: Figure S2). ...
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... relationships in the egg-and-bacon peas differed between estimates using cpDNA and ITS, resulting in slightly different reconstructions of transi- tions between bee-and bird-pollination syndromes (Additional file 1: Figure S1 and Additional file 2: Figure S2). This uncertainty in reconstructing shifts of pollinator syndrome is centred around relationships within Gastrolobium, many of which do not have strong support (Additional file 1: Figure S1 and Additional file 2: Figure S2). The single inferred re- versal in analyses of cpDNA involved a transition back to bee-pollination syndrome in G. pyramidale ( Figure 5), but this node is not well supported and the alternative resolution, in which G. pyramidale is sister to a clade of bird-pollination syndrome species instead of within the clade, is not rejected. ...
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... single inferred re- versal in analyses of cpDNA involved a transition back to bee-pollination syndrome in G. pyramidale ( Figure 5), but this node is not well supported and the alternative resolution, in which G. pyramidale is sister to a clade of bird-pollination syndrome species instead of within the clade, is not rejected. The five or six reversals inferred in ITS analyses are also within Gastrolobium and do not have strong support (Additional file 1: Figure S1 and Additional file 2: Figure S2). has low resolution and in the cpDNA analysis, G. alternifolium is placed with bee-pollination syndrome species (Additional file 1: Figure S1 and Additional file 2: Figure S2). ...
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... five or six reversals inferred in ITS analyses are also within Gastrolobium and do not have strong support (Additional file 1: Figure S1 and Additional file 2: Figure S2). has low resolution and in the cpDNA analysis, G. alternifolium is placed with bee-pollination syndrome species (Additional file 1: Figure S1 and Additional file 2: Figure S2). In all reconstructions, there were many more inferred shifts from bee-to bird-pollination syndrome than the reverse (Table 1). ...

Citations

... Interestingly, bee-pollinated species within this cluster, akin to those in the Horridocactus section, exhibit greater genetic isolation compared with bird-pollinated species, underscoring the influence of pollination mode on genetic differentiation (Villalobos-Barrantes et al., 2022;Walter et al., 2024). This phenomenon might be attributable to the greater dispersal capacity by bird pollinators, resulting in higher levels of connectivity among populations and reduced chances of allopatric isolation and promoting secondary contact (Fernández et al., 2011;Toon et al., 2014;Williamson and Witt, 2021;Dellinger et al., 2022). Historically, this flower morphology has led botanists to place these species within the clade Horridocactus (Kattermann, 1994), but recent plastid and nuclear data robustly support their placement within Neoporteria (Guerrero et al., 2019c). ...
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Background and Aims Pleistocene climatic oscillations, characterized by arid (interglacial) and pluvial (glacial) phases, have profoundly impacted the floras of Mediterranean climates. Our study investigates the hypothesis that these climatic extremes have promoted phases of range expansion and contraction in the Eriosyce sect. Neoporteria, resulting in pronounced genetic structuring and restricted gene flow. Methods Utilizing nuclear microsatellite markers, we genotyped 251 individuals across 18 populations, encompassing all 14 species and one subspecies within the Eriosyce sect. Neoporteria. Additionally, Species Distribution Models (SDMs) were employed to reconstruct past (Last Interglacial, Last Glacial Maximum, Mid-Holocene) and current potential distribution patterns, aiming to delineate the climatic influences on species' range dynamics. Key Results The gene flow analysis disclosed disparate levels of genetic interchange among species, with marked restrictions observed between entities that are geographically or ecologically separated. Notably, E. subgibbosa from Hualpen emerged as genetically distinct, warranting its exclusion for clearer genetic clustering into north, central, and south clusters. The SDMs corroborated these findings, showing marked range expansions during warmer periods and contractions during colder times, indicating significant shifts in distribution patterns in response to climatic changes. Conclusions Our findings emphasize the critical role of Pleistocene climatic fluctuations in driving the dynamic patterns of range expansions and contractions that have led to geographic isolation and speciation within the Eriosyce sect. Neoporteria. Even in the face of ongoing gene flow, these climate-driven processes have played a pivotal role in sculpting the species' genetic architecture and diversity. This study elucidates the complex interplay between climatic variability and evolutionary dynamics among Mediterranean cacti in central Chile, highlighting the necessity of considering historical climatic millenial oscillations in conservation and evolutionary biology studies.
... Although the generality of pollination syndrome showed excellent predictive capability in angiosperms for studying such interactions [17]. On the contrary, this concept has often been questioned by various researchers mentioning other factors responsible for these interactions [15,[18][19][20]. ...
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Genus Buddleja comprises more than 100 subspecies ranging from evergreen to deciduous flowering plants endemic to the USA, Asia, and Africa flourishes from temperate to tropical climatic regions. Most species are known for their luring, aesthetic, scented flowers accustomed as ornamental plants for gardens and their attractiveness towards butterflies, bees, and moths made them special altruists in eliciting pollination. Floral traits and scent composition of several Buddleja species emerged as a fascinating tool to study plant-pollinator interactions in this genus. Benzenoids, oxoisophorone, monoterpenoids, sesquiterpenoids, aldehydes, ketones, and fatty acid derivatives present in the floral scents of Buddleja serve as magnets for pollinators. The present review is of its first kind highlighting the plant-pollinator interactions with emphasis on floral compositions concerning the genus Buddleja.
... The dramatic changes in floral architecture within Harpalyce were likely driven by specialized interactions with pollinators including both bees and birds (Arroyo, 1976). Independent evolutionary shifts from insect to bird pollination have been variously reported across the papilionoid legumes, especially in the neotropical tribe Diocleae and the Australian tribes Mirbelieae and Bossiaeeae (Toon et al., 2014). In all these lineages, evolutionary shifts to bird pollination have also drastically reshaped the floral architecture, substantially deviating from the ancestral morphology where traits are often associated with bee pollination. ...
... The dramatic changes in floral architecture within Harpalyce were likely driven by specialized interactions with pollinators including both bees and birds (Arroyo, 1976). Independent evolutionary shifts from insect to bird pollination have been variously reported across the papilionoid legumes, especially in the neotropical tribe Diocleae and the Australian tribes Mirbelieae and Bossiaeeae (Toon et al., 2014). In all these lineages, evolutionary shifts to bird pollination have also drastically reshaped the floral architecture, substantially deviating from the ancestral morphology where traits are often associated with bee pollination. ...
... Indeed, Michener (1965) referred to Australia as having the most distinctive bee fauna in the world, with one family (Stenotritidae) being entirely restricted to Australia while two other families (Andrenidae and Melittidae) are entirely absent Danforth et al. 2006). Much of the diversity we observe in Australian flowering plants today is associated with interactions involving bees (Toon et al. 2014), and these bees can play critical pollinator roles (Gross and Mackay 1998;Houston 2018;Taylor and Whelan 2014). ...
Article
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Plant-bee networks are rarely, if ever, studied quantitatively at continental scales, yet these have the potential to inform how biota and ecosystems are assembled beyond narrower regional biomes. The short-tongued bee family Colletidae comprises the major component of bee diversity in Australia, with three key subfamilies: the Neopasiphaeinae, Hylaeinae, and Euryglossinae. We use museum data (> 27,000 records) to record binary interactions between these bees (from each of these subfamilies, resolved to subgenera) and plants (resolved to genera). The resulting networks were analysed using bipartite graphs and associated indices of network structure. The three bee subfamilies showed markedly different network structures with their floral hosts. Euryglossinae had strong interactions with Myrtaceae and an otherwise relatively narrow host breadth, Neopasiphaeinae had little signal of host specialisation above genera and a very broad host breadth, and Hylaeinae appeared intermediate in network structure. Furthermore, Euryglossinae is more speciose within Australia (404 species, or ~ 25% of described Australian bee fauna) than Hylaeinae and Neopasiphaeinae, but these differences do not correspond to the stem ages of the three subfamilies, suggesting that time-since-origin does not explain bee species diversity or floral host breadth. Patterns of host breadth persist after rarefaction analyses that correct for differing numbers of observation records. We suggest that visitation networks could be influenced by evolutionary constraints to expansion of floral host breadth, but it is also possible that many bee-plant interactions are shaped by bees exploiting floral traits that are driven by non-bee fauna operating at large biogeographical scales. Euryglossinae / Hylaeinae / Neopasiphaeinae / Pollination / Myrtaceae
... flying vertebrates, large bees), in contrast, may promote outcrossing and gene flow over larger geographic distances (Hughes et al. 2007, Whelan et al. 2009, Ballesteros-Mejia et al. 2016, Gamba & Muchhala 2020. Understanding the extent to which different animal pollinators drive genetic differentiation, ultimately affecting the potential for adaptive evolution and speciation, is essential for better resolving macroevolutionary processes of angiosperm diversification, but it is also of major relevance for choosing appropriate management strategies in human-altered landscapes and under current climate change (Hadley et al. 2012, Toon et al. 2014, Castilla et al. 2017. Surprisingly, however, the impact of different pollination strategies on population genetic parameters across related plant species (accounting for shared macroevolutionary background) has rarely been assessed (Barbará et al. 2007, Kramer et al. 2011. ...
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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. Comparatively investigating how these multifarious factors drive microevolutionary histories is, however, crucial for better resolving macroevolutionary patterns of plant diversification. We here 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 geographic distance, topographic barriers and historic 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.
... Subsequent studies used DNA sequences to estimate the phylogeny and interpreted the morphology from its fit to the molecular trees. A molecular phylogenetic framework for understanding taxonomic limits of the tribes has only partially been developed [34,36,[42][43][44][45][46][47][48]. Both chloroplast DNA sequences (especially trnL-F) and nuclear ribosomal DNA (mainly ITS) have been used and are often combined for analysisexcept when conflicting (e.g., [34,48]). ...
... A molecular phylogenetic framework for understanding taxonomic limits of the tribes has only partially been developed [34,36,[42][43][44][45][46][47][48]. Both chloroplast DNA sequences (especially trnL-F) and nuclear ribosomal DNA (mainly ITS) have been used and are often combined for analysisexcept when conflicting (e.g., [34,48]). Molecular studies have consistently found both Bossiaeeae and core Mirbelieae to be monophyletic. ...
... and Viminaria Sm., have giant antipodals. Relationships among the genera of the giant antipodals group (including Bossiaeeae) have varied among analyses, and also between the genomes [46,48]. This group has usually been found to be non-monophyletic with core Mirbelieae nested inside. ...
Article
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Australia has a very diverse pea-flowered legume flora with 1715 native and naturalised species currently recognised. Tribe Mirbelieae s.l. includes 44% of Australia’s peas in 24 genera with 756 recognised species. However, several genera within the Pultenaea alliance in tribe Mirbelieae are considered to be non-monophyletic and two main options have been proposed: option one is to merge ca. 18 genera containing ca. 540 species (the largest genus, Pultenaea has nomenclatural priority); and option two is to re-circumscribe some genera and describe new genera as required to form monophyletic groups. At the species level, option one would require 76% of names to be changed; whereas based on available data, option two is likely to require, at most, 8.3% of names to change. Option two therefore provides the least nomenclatural disruption but cannot be implemented without a robust phylogenetic framework to define new generic limits. Here we present novel analyses of available plastid DNA data (trnL-F) which suggest that option two would be feasible once sufficient data are generated to resolve relationships. However, the reticulate evolutionary histories or past rapid speciation suggested for this group may prevent the resolution of all nodes. We propose targeted use of Next-Generation Sequencing technology as the best way to resolve relationships between the key clades in the tribe and present a framework for such a study. An overview of current taxonomy in the tribe is presented, along with the state of taxonomic knowledge and availability of published descriptions for electronic flora treatments. Several new combinations and typifications are published in an appendix.
... The ability of such "generalist" pollination systems to transition to most other systems is well-documented in the literature (van der Niet and Johnson 2012). However, we provide another case study demonstrating shifts from highly specialized to more generalized pollination systems, including the transition from bird to bee-pollination (Tripp and Manos 2008;Martén-Rodríguez et al. 2010;Mast et al. 2012;van der Niet and Johnson 2012;Toon et al. 2014;Serrano-Serrano et al. 2017;Kriebel et al. 2019Kriebel et al. , 2020. ...
Article
Natural selection by pollinators is an important factor in the morphological diversity and adaptive radiation of flowering plants. Selection by similar pollinators in unrelated plants leads to convergence in floral morphology, or “floral syndromes.” Previous investigations into floral syndromes have mostly studied relatively small and/or simple systems; emphasizing vertebrate‐pollination. Despite the importance of multiple floral traits in plant‐pollinator interactions, these studies have examined few quantitative traits, so their co‐variation and phenotypic integration have been underexplored. To gain better insights into pollinator‐trait dynamics, we investigate the model system of the phlox family (Polemoniaceae), a clade of ∼ 400 species pollinated by a diversity of vectors. Using a comprehensive phylogeny and large dataset of traits and observations of pollinators, we reconstruct ancestral pollination system; accounting for the temporal history of pollinators. We conduct phylogenetically controlled analyses of trait co‐variation and association with pollinators, integrating many analyses over phylogenetic uncertainty. Pollinator shifts are more heterogeneous than previously hypothesized. The evolution of floral traits is partially constrained by phylogenetic history and trait co‐variation, but traits are convergent and differences are associated with different pollinators. Trait shifts are usually gradual, rather than rapid, suggesting complex genetic and ecological interactions of flowers at macroevolutionary scales. This article is protected by copyright. All rights reserved
... We currently lack additional phylogenetic comparative studies for plants in this region, although a nonstatistical survey of hummingbird-adapted lineages in North America found that transitions from insect to hummingbird pollination are rarely followed by species diversification (Abrahamczyk & Renner, 2015). Reduced diversification for bird pollination compared to insect pollination has also been detected in Australian legume tribes Mirbelieae and Bossiaeae (Toon et al., 2014), and in a broad survey of plants native to New Zealand (Jesson, 2007). These studies are consistent with the expectation that highly mobile pollinators prevent population genetic differentiation, and provide our best evidence that patterns of pollen dispersal may influence plant diversification rates. ...
Article
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Pollinators influence patterns of plant speciation, and one intuitive hypothesis is that pollinators affect rates of plant diversification through their effects on pollen dispersal. By specifying mating events and pollen flow across the landscape, distinct types of pollinators may cause different opportunities for allopatric speciation. This pollen dispersal‐dependent speciation hypothesis predicts that pollination mode has effects on the spatial context of mating events that scale up to impact population structure and rates of species formation. Here I consider recent comparative studies, including genetic analyses of plant mating events, population structure and comparative phylogenetic analyses, to examine evidence for this model. These studies suggest that highly mobile pollinators conduct greater gene flow within and among populations, compared to less mobile pollinators. These differences influence patterns of population structure across the landscape. However, the effects of pollination mode on speciation rates is less predictable. In some contexts, the predicted effects of pollen dispersal are outweighed by other factors that govern speciation rates. A multiscale approach to examine effects of pollination mode on plant mating system, population structure and rates of diversification is key to determining the role of pollen dispersal on plant speciation for model clades.
... It has been suggested that floral color has co-evolved with pollinators such as birds and bees. Bees tend to be attracted to yellow flowers while birds tend to prefer red flowers due to their different visual sensitivities (Toon et al., 2014). Bee-pollinated plants usually have yellow, white, or blue flowers while bird-pollinated plants usually have red flowers (Toon et al., 2014). ...
... Bees tend to be attracted to yellow flowers while birds tend to prefer red flowers due to their different visual sensitivities (Toon et al., 2014). Bee-pollinated plants usually have yellow, white, or blue flowers while bird-pollinated plants usually have red flowers (Toon et al., 2014). The transition from bee-pollination to birdpollination of Australian egg-and-bacon pea is related to the number of bird species in the geographical region where the plants grow (Toon et al., 2014). ...
... Bee-pollinated plants usually have yellow, white, or blue flowers while bird-pollinated plants usually have red flowers (Toon et al., 2014). The transition from bee-pollination to birdpollination of Australian egg-and-bacon pea is related to the number of bird species in the geographical region where the plants grow (Toon et al., 2014). The yellow color of the Lotus flower, together with the orientation, size, petal morphology, sucrose-dominant nectar composition, and scent of the flower, was reported as a factor contributing to the transition to pollination by birds (Cronk and Ojeda, 2008). ...
Article
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Legumes are rich in secondary metabolites, such as polyphenols, alkaloids, and saponins, which are important defense compounds to protect the plant against herbivores and pathogens, and act as signaling molecules between the plant and its biotic environment. Legume-sourced secondary metabolites are well known for their potential benefits to human health as pharmaceuticals and nutraceuticals. During domestication, the color, smell, and taste of crop plants have been the focus of artificial selection by breeders. Since these agronomic traits are regulated by secondary metabolites, the basis behind the genomic evolution was the selection of the secondary metabolite composition. In this review, we will discuss the classification, occurrence, and health benefits of secondary metabolites in legumes. The differences in their profiles between wild legumes and their cultivated counterparts will be investigated to trace the possible effects of domestication on secondary metabolite compositions, and the advantages and drawbacks of such modifications. The changes in secondary metabolite contents will also be discussed at the genetic level to examine the genes responsible for determining the secondary metabolite composition that might have been lost due to domestication. Understanding these genes would enable breeding programs and metabolic engineering to produce legume varieties with favorable secondary metabolite profiles for facilitating adaptations to a changing climate, promoting beneficial interactions with biotic factors, and enhancing health-beneficial secondary metabolite contents for human consumption.