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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Evolutionary convergence on hummingbird pollination in Neotropical Costus provides insight into the causes of pollinator shifts
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 ( 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 in
- NSF-PAR ID:
- 10392935
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 236
- Issue:
- 4
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 1572-1583
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Summary Genetic correlations among different components of phenotypes, especially those resulting from pleiotropy, can constrain or facilitate trait evolution. These factors could especially influence the evolution of traits that are functionally integrated, such as those comprising the flower. Indeed, pleiotropy is proposed as a main driver of repeated convergent trait transitions, including the evolution of phenotypically similar pollinator syndromes.
We assessed the role of pleiotropy in the differentiation of floral and other reproductive traits between two species –
Jaltomata sinuosa andJ. umbellata (Solanaceae) – that have divergent suites of floral traits consistent with bee and hummingbird pollination, respectively. To do so, we generated a hybrid population and examined the genetic architecture (trait segregation and quantitative trait locus (QTL ) distribution) underlying 25 floral and fertility traits.We found that most floral traits had a relatively simple genetic basis (few, predominantly additive,
QTL s of moderate to large effect), as well as little evidence of antagonistic pleiotropy (few trait correlations andQTL colocalization, particularly between traits of different classes). However, we did detect a potential case of adaptive pleiotropy among floral size and nectar traits.These mechanisms may have facilitated the rapid floral trait evolution observed within
Jaltomata , and may be a common component of rapid phenotypic change more broadly. -
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Summary Evolution of complex phenotypes depends on the adaptive importance of individual traits, and the developmental changes required to modify traits. Floral syndromes are complex adaptations to pollinators that include color, nectar, and shape variation. Hummingbird‐adapted flowers have evolved a remarkable number of times from bee‐adapted ancestors in
Penstemon , and previous work demonstrates that color over shape better distinguishes bee from hummingbird syndromes. Here, we examined the relative importance of nectar volume and nectary development in definingPenstemon pollination syndromes.We tested the evolutionary association of nectar volume and nectary area with pollination syndrome across 19
Penstemon species. In selected species, we assessed cellular‐level processes shaping nectary size. Within a segregating population from an intersyndrome cross, we assessed trait correlations between nectar volume, nectary area, and the size of stamens on which nectaries develop.Nectar volume and nectary area displayed an evolutionary association with pollination syndrome. These traits were correlated within a genetic cross, suggesting a mechanistic link. Nectary area evolution involves parallel processes of cell expansion and proliferation.
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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 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 ofC. 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. -
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In the formation of species, adaptation by natural selection generates distinct combinations of traits that function well together. The maintenance of adaptive trait combinations in the face of gene flow depends on the strength and nature of selection acting on the underlying genetic loci. Floral pollination syndromes exemplify the evolution of trait combinations adaptive for particular pollinators. The North American wildflower genus
Penstemon displays remarkable floral syndrome convergence, with at least 20 separate lineages that have evolved from ancestral bee pollination syndrome (wide blue-purple flowers that present a landing platform for bees and small amounts of nectar) to hummingbird pollination syndrome (bright red narrowly tubular flowers offering copious nectar). Related taxa that differ in floral syndrome offer an attractive opportunity to examine the genomic basis of complex trait divergence. In this study, we characterized genomic divergence among 229 individuals from aPenstemon species complex that includes both bee and hummingbird floral syndromes. Field plants are easily classified into species based on phenotypic differences and hybrids displaying intermediate floral syndromes are rare. Despite unambiguous phenotypic differences, genome-wide differentiation between species is minimal. Hummingbird-adapted populations are more genetically similar to nearby bee-adapted populations than to geographically distant hummingbird-adapted populations, in terms of genome-wided XY . However, a small number of genetic loci are strongly differentiated between species. These approximately 20 “species-diagnostic loci,” which appear to have nearly fixed differences between pollination syndromes, are sprinkled throughout the genome in high recombination regions. Several map closely to previously established floral trait quantitative trait loci (QTLs). The striking difference between the diagnostic loci and the genome as whole suggests strong selection to maintain distinct combinations of traits, but with sufficient gene flow to homogenize the genomic background. A surprisingly small number of alleles confer phenotypic differences that form the basis of species identity in this species complex.
