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Floral Scents of a Deceptive Plant Are Hyperdiverse and Under Population-Specific Phenotypic Selection.

ABSTRACT: Floral scent is a key mediator in plant-pollinator interactions. However, little is known to what extent intraspecific scent variation is shaped by phenotypic selection, with no information yet in deceptive plants. In this study, we collected inflorescence scent and fruit set of the deceptive moth fly-pollinated Arum maculatum L. (Araceae) from six populations north vs. five populations south of the Alps, accumulating to 233 samples in total, and tested for differences in scent, fruit set, and phenotypic selection on scent across this geographic barrier. We recorded 289 scent compounds, the highest number so far reported in a single plant species. Most of the compounds occurred both north and south of the Alps; however, plants of the different regions emitted different absolute and relative amounts of scent. Fruit set was higher north than south of the Alps, and some, but not all differences in scent could be explained by differential phenotypic selection in northern vs. southern populations. This study is the first to provide evidence that floral scents of a deceptive plant are under phenotypic selection and that phenotypic selection is involved in shaping geographic patterns of floral scent in such plants. The hyperdiverse scent of A. maculatum might result from the imitation of various brood substrates of its pollinators.

SUBMITTER: Gfrerer E

PROVIDER: S-EPMC8500232 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Floral Scents of a Deceptive Plant Are Hyperdiverse and Under Population-Specific Phenotypic Selection.

Gfrerer Eva E Laina Danae D Gibernau Marc M Fuchs Roman R Happ Martin M Tolasch Till T Trutschnig Wolfgang W Hörger Anja C AC Comes Hans Peter HP Dötterl Stefan S

Frontiers in plant science 20210924

Floral scent is a key mediator in plant-pollinator interactions. However, little is known to what extent intraspecific scent variation is shaped by phenotypic selection, with no information yet in deceptive plants. In this study, we collected inflorescence scent and fruit set of the deceptive moth fly-pollinated <i>Arum maculatum</i> L. (Araceae) from six populations north vs. five populations south of the Alps, accumulating to 233 samples in total, and tested for differences in scent, fruit set ...[more]

PMID: 34630465

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Project description:Currently, a global analysis of the information available on the relative composition of the floral scents of a very diverse variety of plant species is missing. Such analysis may reveal general patterns on the distribution and dominance of the volatile compounds that form these mixtures, and may also allow measuring the effects of factors such as the phylogeny, pollination vectors, and climatic conditions on the floral scents of the species. To fill this gap, we compiled published data on the relative compositions and emission rates of volatile organic compounds (VOCs) in the floral scents of 305 plant species from 66 families. We also gathered information on the groups of pollinators that visited the flowers and the climatic conditions in the areas of distribution of these species. This information allowed us to characterize the occurrence and relative abundances of individual volatiles in floral scents and the effects of biotic and climatic factors on floral scent. The monoterpenes trans-β-ocimene and linalool and the benzenoid benzaldehyde were the most abundant floral VOCs, in both ubiquity and predominance in the floral blends. Floral VOC richness and relative composition were moderately preserved traits across the phylogeny. The reliance on different pollinator groups and the climate also had important effects on floral VOC richness, composition, and emission rates of the species. Our results support the hypothesis that key compounds or compounds originating from specific biosynthetic pathways mediate the attraction of the main pollinators. Our results also indicate a prevalence of monoterpenes in the floral blends of plants that grow in drier conditions, which could link with the fact that monoterpene emissions protect plants against oxidative stresses throughout drought periods and their emissions are enhanced under moderate drought stress. Sesquiterpenes, in turn, were positively correlated with mean annual temperature, supporting that sesquiterpene emissions are dominated mainly by ambient temperature. This study is the first to quantitatively summarise data on floral-scent emissions and provides new insights into the biotic and climatic factors that influence floral scents.

Project description:Background and aimsThe deception strategies of orchids remain poorly understood, especially in regard to the chemical compounds emitted from their flowers and their interaction with various taxonomic groups of pollinators. We investigated the phylogenetic relationships and compared the variation of floral chemical compounds between food-deceptive Dactylorhiza taxa (D. incarnata var. incarnata and D. incarnata var. ochroleuca, D. fuchsii and D. majalis) from populations in north-eastern Poland. We propose a model of the evolution of deception based on floral chemical signals in this genus.MethodsA Bayesian approach based on polymorphic plastid DNA (trnL, trnF and psbC-trnK), internal transcribed spacer (ITS) sequences and flow cytometry data was applied to confirm the taxonomic status of the studied orchids. We also identified and classified the pollinators and flower visitors in each Dactylorhiza population to the taxonomic level and compared our results with literature data. The chemical composition of pentane and diethyl ether extracts from the flowers was analysed by gas chromatography-mass spectrometry. Variation of the floral chemical components was visualized by non-metric multidimensional scaling based on Bray-Curtis dissimilarity.Key resultsThe genetic distinctiveness of D. incarnata, D. fuchsii and D. majalis was confirmed. No hybrids between them were found, but the chloroplast DNA (cpDNA), ITS haplotypes and flow cytometry showed genetic similarity between D. incarnata var. incarnata and D. incarnata var. ochroleuca. We determined that Apis mellifera (Hymenoptera) was the only shared pollinator of these taxa. Strangalia attenuata and Alosterna tabacicolor (Coleoptera) and Volucella pellucens and V. bombylans (Hymenoptera) were observed pollinating D. fuchsii. Visualization of the emission rates of the 61 floral chemical compounds detected from pentane extracts (mainly hydrocarbons and aldehydes) and the 51 from diethyl extracts (with abundant groups of benzenoids and non-aromatic acids) strongly differentiated D. incarnata, D. fuchsii and D. majalis, while those of the two varieties of D. incarnata (var. incarnata and var. ochroleuca) were almost identical.ConclusionsWhile the genetic data clearly supported the distinct lineages of D. incarnata, D. fuchsii and D. majalis, the patterns of emission of their flower chemical compounds were more complex within the series of shared compounds (alkanes and aldehydes) and taxon-specific compounds (benzenoids and esters). Their floral bouquet can influence the sexual, social and feeding behaviour of pollinators in different ways. We observed that the floral chemical compounds attracted both shared and species-specific pollinators to Dactylorhiza, confirming the multidirectional character of floral chemical signals in these food-deceptive taxa. Reduction of species-specific pollination levels in Dactylorhiza orchid taxa may promote hybridization between them.

Dataset Information

Floral Scents of a Deceptive Plant Are Hyperdiverse and Under Population-Specific Phenotypic Selection.

Publications

Floral Scents of a Deceptive Plant Are Hyperdiverse and Under Population-Specific Phenotypic Selection.

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