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Combinations of correlated floral traits have arisen repeatedly across angiosperms through convergent evolution in response to pollinator selection to optimize reproduction. While some plant groups exhibit very distinct combinations of traits adapted to specific pollinators (so-called pollination syndromes), others do not. Determining how floral traits diverge across clades and whether floral traits show predictable correlations in diverse groups of flowering plants is key to determining the extent to which pollinator-mediated selection drives diversification. The North AmericanSilenesectionPhysolychnisis an ideal group to investigate patterns of floral evolution because it is characterized by the evolution of novel red floral color, extensive floral morphological variation, polyploidy, and exposure to a novel group of pollinators (hummingbirds). We test for correlated patterns of trait evolution that would be consistent with convergent responses to selection in the key floral traits of color and morphology. We also consider both the role of phylogenic distance and geographic overlap in explaining patterns of floral trait variation. Inconsistent with phenotypically divergent pollination syndromes, we find very little clustering of North AmericanSileneinto distinct floral morphospace. We also find little evidence that phylogenetic history or geographic overlap explains patterns of floral diversity in this group. White- and pink-flowering species show extensive phenotypic diversity but are entirely overlapping in morphological variation. However, red-flowering species have much less phenotypic disparity and cluster tightly in floral morphospace. We find that red-flowering species have evolved floral traits that align with a traditional hummingbird syndrome, but that these trait values overlap with several white and pink species as well. Our findings support the hypothesis that convergent evolution does not always proceed through comparative phenotypic divergence, but possibly through sorting of standing ancestral variation.
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Phylogenomics and macroevolution of a florally diverse Neotropical plant clade
Abstract Hillieae is a group of ∼30 florally diverse, Neotropical epiphyte species. Species richness peaks in southern Central America and taxa display bat, hawkmoth, or hummingbird pollination syndromes. A phylogenetic framework is needed to understand floral and biogeographic evolution. We used target enrichment data to infer a species tree and a Bayesian time-calibrated tree including ∼83% of the species in the group. We inferred ancestral biogeography and pollination syndromes, described species’ realized bioclimatic niches via a principal component analysis, and estimated significant niche shifts using Ornstein–Uhlenbeck models to understand how different abiotic and biotic variables have shaped Hillieae evolution. We estimated that Hillieae originated in southern Central America 19 Ma and that hawkmoth pollination is the ancestral character state. Multiple independent shifts in pollination syndrome, biogeographic distribution, and realized bioclimatic niche have occurred, though bioclimatic niche is largely conserved. Using generalized linear models, we identify two interactions—between species’ biogeographic ranges and pollination syndromes, and between phylogenetic covariance and pollination syndromes—that additively affect the degree of bioclimatic niche overlap between species. Regional variation in pollination syndrome diversity and patterns of species bioclimatic niche overlap indicate a link between biogeography and species ecology in driving Hillieae diversification and syndrome evolution.
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- Award ID(s):
- 2055525
- PAR ID:
- 10611499
- Editor(s):
- Borges, Diogo; Morlon, Hélène
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Evolution
- ISSN:
- 0014-3820
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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‘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
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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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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/evolut/qpaf099
