Deceptive strategy in Dactylorhiza orchids: multidirectional evolution of floral chemistry

Abstract

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.• Methods A 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 nonaromatic 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.• Conclusions While 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.

What are the drivers of female success in food‐deceptive orchids?

“…It may strengthen associative learning and thus encourage repeat visitation by pollinators (Knudsen & Gershenzon, 2006). Wróblewska et al (2019) reported that the floral chemical compounds in studied D. incarnata populations were dominated by aldehydes and n-alkanes/alkenes, and the benzoids.…”

“…The Dactylorhiza genus is recognized as food-deceptive orchids, and it has been used as a model for investigating plant-pollinator interactions, natural selection, and, consequent female reproductive success (Mattila & Kuitunen, 2000;Sletvold et al, 2010;Trunschke et al, 2017). The study of Wróblewska et al (2019)…”

Pollinators and visitors of the generalized food-deceptive orchid Dactylorhiza majalis in North-Eastern Poland

“…The reason why A. mellifera and potentially other insects can be lured by D. majalis is the floral chemical compounds released by D. majalis, which were reported by Wróblewska et al (2019) in populations from north-eastern Poland. These chemical compounds include p-hydroxybenzyl alcohol (a volatile compound in Vanilla, describing it as vanilla-like), and aldehydes (which are important components of floral odor in the appetitive proboscis extension response in honey bees, Wang et al 2016), particularly nonanal.…”

Traditional, Therapeutic Uses and Phytochemistry of Terrestrial European Orchids and Implications for Conservation

“…This may depend on several aspects, including the extraction methods and the analytical tools chosen [ 20 , 254 , 255 ]. For instance, more polar compounds such as polyphenols are less volatiles and therefore the use of protic solvents (such as methanol, diethyl ether or water–ethanol) results in substantially different chemical characterizations in respect to dynamic headspace sorption methods (i.e., [ 176 , 185 , 192 ]). Individual situations also contribute to changing metabolic processes and thus varying phytochemical profiles.…”