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Summary The evolution of hummingbird pollination is common across angiosperms throughout the Americas, presenting an opportunity to examine convergence in both traits and environments to better understand how complex phenotypes arise. Here we examine independent shifts from bee to hummingbird pollination in the Neotropical spiral gingers (Costus) and address common explanations for the prevalence of transitions from bee to hummingbird pollination.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 correlate with elevation or climate.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 climate.Evolutionary shifts to hummingbird pollination inCostusare highly convergent and directional, involve a surprising set of traits when compared with other plants with analogous transitions and refute the generality of several common explanations for the prevalence of transitions from bee to hummingbird pollination.
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Within-species floral evolution reveals convergence in adaptive walks during incipient pollinator shift
Abstract Understanding how evolution proceeds from molecules to organisms to interactions requires integrative studies spanning biological levels. Linking phenotypes with associated genes and fitness illuminates how adaptive walks move organisms between fitness peaks. Floral evolution can confer rapid reproductive isolation, often converging in association with pollinator guilds. Within the monkeyflowers (Mimulussect.Erythranthe), yellow flowers within red hummingbird-pollinated species have arisen at least twice, suggesting possible pollinator shifts. We compare two yellow-flowered forms ofM. cardinalisandM. verbenaceusto their red counterparts in floral phenotypes, biochemistry, transcriptomic and genomic variation, and pollinator interactions. We find convergence in ongoing adaptive walks of both yellow morphs, with consistent changes in traits of large effect (floral pigments, associated gene expression), resulting in strong preference for yellow flowers by bumblebees. Shifts in scent emission and floral opening size also favor bee adaptation, suggesting smaller-effect steps from hummingbird to bee pollination. By examining intraspecific, incipient pollinator shifts in two related species, we elucidate adaptive walks at early stages, revealing how convergent large effect mutations (floral color) may drive pollinator attraction, followed by smaller effect changes for mechanical fit and reward access. Thus, ongoing adaptive walks may impact reproductive isolation and incipient speciation via convergent evolution.
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- Award ID(s):
- 2208984
- PAR ID:
- 10578227
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 16
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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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
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