An official website of the United States government
PremiseVariation in pollen‐ovule ratios is thought to reflect the degree of pollen transfer efficiency—the more efficient the process, the fewer pollen grains needed. Few studies have directly examined the relationship between pollen‐ovule ratio and pollen transfer efficiency. For active pollination in the pollination brood mutualisms of yuccas and yucca moths, figs and fig wasps, senita and senita moths, and leafflowers and leafflower moths, pollinators purposefully collect pollen and place it directly on the stigmatic surface of conspecific flowers. The tight coupling of insect reproductive interests with pollination of the flowers in which larvae develop ensures that pollination is highly efficient. MethodsWe used the multiple evolutionary transitions between passive pollination and more efficient active pollination to test if increased pollen transfer efficiency leads to reduced pollen‐ovule ratios. We collected pollen and ovule data from a suite of plant species from each of the pollination brood mutualisms and used phylogenetically controlled tests and sister‐group comparisons to examine whether the shift to active pollination resulted in reduced pollen‐ovule ratios. ResultsAcross all transitions between passive and active pollination in plants, actively pollinated plants had significantly lower pollen‐ovule ratios than closely related passively pollinated taxa. Phylogenetically corrected comparisons demonstrated that actively pollinated plant species had an average 76% reduction in the pollen‐ovule ratio. ConclusionsThe results for active pollination systems support the general utility of pollen‐ovule ratios as indicators of pollination efficiency and the central importance of pollen transfer efficiency in the evolution of pollen‐ovule ratio.
more »
« less
A lever action hypothesis for pendulous hummingbird flowers: experimental evidence from a columbine
Abstract Background and AimsPendulous 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. MethodsTo 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 ResultsSeed 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. ConclusionsWe 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.
more »
« less
- Award ID(s):
- 1831164
- PAR ID:
- 10130134
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Annals of Botany
- Volume:
- 125
- Issue:
- 1
- ISSN:
- 0305-7364
- Page Range / eLocation ID:
- p. 59-65
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract PremiseA switch in pollinator can occur when a plant lineage enters a new habitat where the ancestral pollinator is less common, and a novel pollinator is more common. Because pollinator communities vary according to environmental tolerances and availability of resources, there may be consistent associations between pollination mode and specific regions and habitats. Such associations can be studied in lineages that have experienced multiple pollinator transitions, representing evolutionary replicates. MethodsOur study focused on a large clade ofPenstemonwildflower species in western North America, which has repeatedly evolved hummingbird‐adapted flowers from ancestral bee‐adapted flowers. For each species, we estimated geographic ranges from occurrence data and inferred environmental niches from climate, topographical, and soil data. Using a phylogenetic comparative approach, we investigated whether hummingbird‐adapted species occupy distinct geographic regions or habitats relative to bee‐adapted species. ResultsHummingbird‐adapted species occur at lower latitudes and lower elevations than bee‐adapted species, resulting in a difference in their environmental niche. Bee‐adapted species sister to hummingbird‐adapted species are also found in relatively low elevations and latitudes, similar to their hummingbird‐adapted sister species, suggesting ecogeographic shifts precede pollinator divergence. Sister species pairs—regardless of whether they differ in pollinator—show relatively little geographic range overlap. ConclusionsAdaptation to a novel pollinator may often occur in geographic and ecological isolation from ancestral populations. The ability of a given lineage to adapt to novel pollinators may critically depend on its ability to colonize regions and habitats associated with novel pollinator communities.more » « less
-
Abstract PremiseCentropogonsubgenusCentropogoncomprises 55 species found primarily in midelevation Andean forests featuring some of the most curved flowers among angiosperms. Floral curvature is linked to coevolution with the sicklebill hummingbird, which pollinates most species. Despite charismatic flowers, there is limited knowledge about the phylogenetic relationships and floral evolution. MethodsWe conducted the first densely sampled phylogenomic analysis of the clade using methods that account for incomplete lineage sorting on a sequence capture dataset generated with a lineage‐specific probe set. Using phylogenetic comparative methods, we test for correlated evolution of two traits central to sicklebill pollination. ResultsWe improve understanding of species relationships by more than doubling past taxon sampling. We confirm the monophyly of the subgenus and two sections, and the non‐monophyly of remaining sections. The subgenus is characterized by high gene tree discordance. Three widespread species display contrasting phylogenetic dynamics, withC. cornutusforming a clade andC. granulosusandC. solanifoliusforming non‐monophyletic, biogeographically clustered lineages. Correlated evolution of floral curvature and inflorescence structure has led to multiple putative losses of sicklebill pollination. ConclusionsCentropogonsubgenusCentropogonadds to a growing body of literature of Andean plant clades with high gene tree discordance. This phylogeny serves as a foundational framework for further macroevolutionary investigations into the environmental and biogeographic factors shaping the evolution of pollination‐related traits.more » « less
-
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.more » « less
-
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
