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On the success of a swindle: pollination by deception in orchids

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Abstract

A standing enigma in pollination ecology is the evolution of pollinator attraction without offering reward in about one third of all orchid species. Here I review concepts of pollination by deception, and in particular recent findings in the pollination syndromes of food deception and sexual deception in orchids. Deceptive orchids mimic floral signals of rewarding plants (food deception) or mating signals of receptive females (sexual deception) to attract pollen vectors. In some food deceptive orchids, similarities in the spectral reflectance visible to the pollinator in a model plant and its mimic, and increased reproductive success of the mimic in the presence of the model have been demonstrated. Other species do not mimic specific model plants but attract pollinators with general attractive floral signals. In sexually deceptive orchids, floral odor is the key trait for pollinator attraction, and behaviorally active compounds in the orchids are identical to the sex pheromone of the pollinator species. Deceptive orchids often show high variability in floral signals, which may be maintained by negative frequency-dependent selection, since pollinators can learn and subsequently avoid common deceptive morphs more quickly than rare ones. The evolution of obligate deception in orchids seems paradoxical in the light of the typically lower fruit set than in rewarding species. Pollination by deception, however, can reduce self-pollination and encourage pollen flow over longer distances, thus promoting outbreeding. Although some food deceptive orchids are isolated through postzygotic reproductive barriers, sexually deceptive orchids lack post-mating barriers and species isolation is achieved via specific pollinator attraction. Recent population genetic and phylogenetic investigations suggest gene-flow within subgeneric clades, but pollinator-mediated selection may maintain species-specific floral traits.

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Acknowledgements

I would like to thank Rod Peakall (Canberra), Jim Mant (Zürich), Salvatore Cozzolino (Naples), Manfred Ayasse (Ulm), Wittko Francke (Hamburg), Fernando Ibarra (Hamburg), Claudia Schulz (Hamburg), and Roman Kaiser (Dübendorf) for sharing their insights during many years of fruitful collaboration. Rod Peakall, Jim Mant, Alex Widmer (Zürich), and Salvatore Cozzolino provided helpful comments on this manuscript, and Charlotte Salzmann (Zürich) supplied a picture for this paper. I would also like to thank Peter Linder (Zürich), Amots Dafni (Haifa), Steve Johnson (Pietermaritzburg), and Hannes Paulus (Vienna), for inspiring discussions on the mysteries of orchid pollination. The research of the author is supported by the SNF (3100–68173.02) and ETH Zürich (02297/41-2710)

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Schiestl, F.P. On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92, 255–264 (2005). https://doi.org/10.1007/s00114-005-0636-y

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