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1. The evolution of hummingbird pollination is common across angiosperm lineages throughout the Americas, presenting an opportunity to examine convergence in both traits and environments to better understand how complex phenotypes arise. We examine multiple independent shifts from bee to hummingbird pollination in the Neotropical spiral gingers (Costus) and use our data to address several common explanations for the prevalence of bee to bird pollination transitions. 2. We use floral traits of species with observed pollinators to predict pollinators of unobserved species and reconstruct ancestral pollination states on a well-resolved phylogeny. We examine whether independent transitions evolve towards the same phenotypic optimum and whether shifts to hummingbird pollination are associated with high elevation or climatic niche. 3. Traits predicting hummingbird pollination include small flower size, brightly-colored floral bracts, and the absence of nectar guides. We find many shifts to hummingbird pollination and no reversals, a single shared phenotypic optimum across hummingbird flowers, and no association between pollination and elevation or climatic niche. 4. Costus presents surprising findings compared to other plant clades. Hummingbird flowers are consistently smaller than bee flowers and primary flower colors are not predictive of pollinators. Moreover, hummingbird pollination shows no association with high elevation, as found in other tropical plants.
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A lever action hypothesis for pendulous hummingbird flowers: experimental evidence from a columbine
Abstract Background and Aims Pendulous flowers (due to a flexible pedicel) are a common, convergent trait of hummingbird-pollinated flowers. However, the role of flexible pedicels remains uncertain despite several functional hypotheses. Here we present and test the ‘lever action hypothesis’: flexible pedicels allow pendulous flowers to move upwards from all sides, pushing the stigma and anthers against the underside of the feeding hummingbird regardless of which nectary is being visited. Methods To test whether this lever action increased pollination success, we wired emasculated flowers of serpentine columbine, Aquilegia eximia, to prevent levering and compared pollination success of immobilized flowers with emasculated unwired and wire controls. Key Results Seed set was significantly lower in wire-immobilized flowers than unwired control and wire control flowers. Video analysis of visits to wire-immobilized and unwired flowers demonstrated that birds contacted the stigmas and anthers of immobilized flowers less often than those of flowers with flexible pedicels. Conclusions We conclude that flexible pedicels permit the levering of reproductive structures onto a hovering bird. Hummingbirds, as uniquely large, hovering pollinators, differ from flies or bees which are too small to cause levering of flowers while hovering. Thus, flexible pedicels may be an adaptation to hummingbird pollination, in particular due to hummingbird size. We further speculate that this mechanism is effective only in radially symmetric flowers; in contrast, zygomorphic hummingbird-pollinated flowers are usually more or less horizontally oriented rather than having pendulous flowers and flexible pedicels.
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- Award ID(s):
- 1831164
- PAR ID:
- 10177673
- Date Published:
- Journal Name:
- Annals of Botany
- Volume:
- 125
- Issue:
- 1
- ISSN:
- 0305-7364
- Page Range / eLocation ID:
- 59 to 65
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Background and Aims Wind pollination has evolved repeatedly in flowering plants, yet the identification of a wind pollination syndrome as a set of integrated floral traits can be elusive. Thalictrum (Ranunculaceae) comprises temperate perennial herbs that have transitioned repeatedly from insect to wind pollination while also exhibiting mixed pollination, providing an ideal system to test for evolutionary correlation between floral morphology and pollination mode in a biotic to abiotic continuum. Moreover, the lack of floral organ fusion across this genus additionally allows to test for specialization to pollination vectors in the absence of this feature. Methods We expanded phylogenetic sampling in the genus from a previous study using six chloroplast loci, which allowed us to test whether species cluster into distinct pollination syndromes based on floral morphology. We then used multivariate analyses on floral traits, followed by ancestral state reconstruction of the emerging flower morphotypes and determined whether these traits are evolutionarily correlated under a Bayesian framework with Brownian motion. Key Results Floral traits fell into five distinct clusters, which were reduced to three after considering phylogenetic relatedness, and were largely consistent with flower morphotypes and associated pollination vectors. Multivariate evolutionary analyses found a positive correlation between the lengths of floral reproductive structures (styles, stigmas, filaments, and anthers). Shorter reproductive structures tracked insect-pollinated species and clades in the phylogeny while longer structures tracked wind-pollinated ones, consistent with selective pressures exerted by biotic vs. abiotic pollination vectors, respectively. Conclusions While detectable suites of integrated floral traits across Thalictrum correlated with wind or insect pollination at the extremes of the morphospace distribution, a presumed intermediate, mixed pollination mode morphospace was also detected. Thus, our data broadly support the existence of detectable flower morphotypes from convergent evolution underlying pollination mode evolution in Thalictrum, presumably via different paths from an ancestral mixed pollination state.more » « less
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Summary The evolutionary switch to hummingbird pollination exemplifies complex adaptation, requiring evolutionary change in multiple component traits. Despite this complexity, diverse lineages have converged on hummingbird‐adapted flowers on a relatively short evolutionary timescale. Here, I review how features of the genetic basis of adaptation contribute to this remarkable evolutionary lability. Large‐effect substitutions, large mutational targets for adaptation, adaptive introgression, and concentrated architecture all contribute to the origin and maintenance of hummingbird‐adapted flowers. The genetic features of adaptation are likely shaped by the ecological and geographic context of the switch to hummingbird pollination, with implications for future evolutionary trajectories.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/aob/mcz134
