An official website of the United States government
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.
more »
« less
Stigma shape shifting in sages ( Salvia : Lamiaceae): hummingbirds guided the evolution of New World floral features
Abstract A fundamental question in evolutionary biology is how clades of organisms exert influence on one another. The evolution of the flower and subsequent plant/pollinator coevolution are major innovations that have operated in flowering plants to promote species radiations at a variety of taxonomic levels in the Neotropics. Here we test the hypothesis that pollination by Neotropical endemic hummingbirds drove the evolution of two unique stigma traits in correlation with other floral traits in New World Salvia (Lamiaceae). We examined morphometric shapes of stigma lobing across 400 Salvia spp., scored presence and absence of a stigma brush across Salvia, and used a suite of phylogenetic comparative methods to detect shape regime shifts, correlation of trait shifts with BayesTraits and phylogenetic generalized least square regressions, and the influence of scored pollinators on trait evolution using OUwie. We found that a major Neotropical clade of Salvia evolved a correlated set of stigma features, with a longer upper stigma lobe and stigmatic brush, following an early shift to hummingbird pollination. Evolutionary constraint is evident as subsequent shifts to bee pollination largely retained these two features. Our results support the hypothesis that hummingbirds guided the correlative shifts in corolla, anther connective, style and stigma shape in Neotropical Salvia, despite repeated shifts back to bee pollination.
more »
« less
- Award ID(s):
- 1655606
- PAR ID:
- 10378942
- Date Published:
- Journal Name:
- Botanical Journal of the Linnean Society
- Volume:
- 199
- Issue:
- 1
- ISSN:
- 0024-4074
- Page Range / eLocation ID:
- 428 to 448
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Different populations of plant species can adapt to their local pollinators and diverge in floral traits accordingly. Floral traits are subject to pollinator‐driven natural selection to enhance plant reproductive success. Studies on temperate plant systems have shown pollinator‐driven selection results in floral trait variation along elevational gradients, but studies in tropical systems are lacking. We analyzed floral traits and pollinator assemblages in the Neotropical bee‐pollinated taxonCostus guanaiensisvar.tarmicusacross four sites along a steep elevational gradient in Peru. We found variations in floral traits of size, color, and reward, and in the pollinator assemblage along the elevational gradient. We examined our results considering two hypotheses, (1) local adaptation to different bee assemblages, and (2) the early stages of an evolutionary shift to a new pollinator functional group (hummingbirds). We found some evidence consistent with the adaptation ofC. guanaiensisvar.tarmicusto the local bee fauna along the studied elevational gradient. Corolla width across sites was associated with bee thorax width of the local most frequent pollinator. However, we could not rule out the possibility of the beginning of a bee‐to‐hummingbird pollination shift in the highest‐studied site. Our study is one of the few geographic‐scale analyses of floral trait and pollinator assemblage variation in tropical plant species. Our results broaden our understanding of plant‐pollinator interactions beyond temperate systems by showing substantial intraspecific divergence in both floral traits and pollinator assemblages across geographic space in a tropical plant species.more » « less
-
‘Pollination syndromes’, where convergent floral signals reflect selection from a functional pollinator group, are often characterized by physical features, yet floral rewards such as nectar may also reflect selection from pollinators. We asked whether nectar chemistry shows evidence of convergence across functional pollinator groups, i.e. a ‘chemical pollination syndrome’. We used untargeted metabolomics to compare nectar and leaf chemical profiles across 19 bee‐ and bird‐syndrome species, focusing on Salvia spp. (Lamiaceae), selected to maximize switching events between pollination syndromes.We found that independently derived bird‐syndrome nectar showed convergence on nectar traits distinct from bee‐syndrome nectar, primarily driven by the composition and concentration of alkaloid profiles. We did not find evidence for ‘passive leaking’ of nectar compounds from leaves since metabolite abundances were uncorrelated across tissues and many nectar metabolites were not present in leaves. Nectar and leaf metabolomes were strongly decoupled from phylogenetic relationships within Salvia. These results suggest that functional pollinator groups may drive the evolution of floral reward chemistry, consistent with our ‘chemical pollination syndrome’ hypothesis and indicative of selection by pollinators, but we also consider alternative explanations. In addition, our results support the notion that nectar chemistry can be decoupled from that of other tissues.more » « less
-
Different populations of plant species can adapt to their local pollinators and diverge in floral traits accordingly. Floral traits are subject to pollinator-driven natural selection to enhance plant reproductive success. Studies on temperate plant systems have shown pollinator-driven selection results in floral trait variation along elevational gradients, but studies in tropical systems are lacking. We analyzed floral traits and pollinator assemblages in the Neotropical bee-pollinated taxon Costus guanaiensis var. tarmicus across four sites along a steep elevational gradient in Peru. We found variations in floral traits of size, color, and reward, and in the pollinator assemblage along the elevational gradient. We examined our results considering two hypotheses, (1) local adaptation to different bee assemblages, and (2) the early stages of an evolutionary shift to a new pollinator functional group (hummingbirds). We found some evidence consistent with the adaptation of C. guanaiensis var. tarmicus to the local bee fauna along the studied elevational gradient. Corolla width across sites was associated with bee thorax width of the local most frequent pollinator. However, we could not rule out the possibility of the beginning of a bee-to-hummingbird pollination shift in the highest-studied site. Our study is one of the few geographic-scale analyses of floral trait and pollinator assemblage variation in tropical plant species. Our results broaden our understanding of plant-pollinator interactions beyond temperate systems by showing substantial intraspecific divergence in both floral traits and pollinator assemblages across geographic space in a tropical plant species.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
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/botlinnean/boab096
