Sexual Deception in Orchids

Abstract

Sexual deception has evolved repeatedly within the Orchidaceae. All species exploit the sexual communication system of insects; they rely on a combination of olfactory, visual and tactile signals for tempting mate‐searching males into copulation attempts with their flowers. The exploitation of their pollinator's private communication channel ensures a highly effective pollen transport between conspecific flowers. Despite the elaborate pollination mechanisms deployed by sexually deceptive orchids, their annual reproductive success is notoriously low. This has fuelled intensive research into the evolutionary mechanisms which have given rise to sexual deception. Existing evidence support the hypothesis that these orchids have traded high reproductive output for higher quality seed production. But other factors may also be involved. While their evolution remains shrouded in mystery, their diversification has been revealed to be linked to repeated pollinator shifts mediated by the malleability of their floral traits. Despite decades of research, sexual deception still poses unanswered questions.

Key Concepts

  • Sexually deceptive orchids rely on mimicking the chemical, visual and tactile cues used by female insects to attract mate‐searching males. The mimicry is highly accurate, making it difficult for males to distinguish between their conspecific females and the orchid flowers.
  • Sexual deception is a highly specific pollination system; each orchid being usually pollinated by a single pollinator species.
  • The specific pollinator attraction is mediated by the same combination of flower traits in most sexually deceptive species. The sexual pheromone analogue produced by the flowers is thereby the key trait involved in ensuring specific pollinator attraction.
  • Flower colour and morphology can also play a crucial role in pollinator attraction and in ensuring that the pollinators will contact the reproductive structures of the flowers.
  • Despite their elaborate pollination strategies, sexually deceptive orchids are notorious for their low reproductive success. Low fruiting success seems, however, to be compensated by the production of high‐quality seeds through higher outcrossing rates than their food deceptive relatives.
  • It is still debated how and why sexually deceptive orchids evolved from their food‐deceptive ancestors. There are multiple hypotheses which could explain the evolution of sexual deception, but a clear pattern has not yet emerged.
  • Despite their low reproductive success, sexually deceptive orchids seem to be evolutionary highly successful. Their diversification has been linked to repeated pollinator‐shifts driven by often minute changes in their sexual pheromone analogues, followed by subsequent alterations of their flower colour and morphology.

Keywords: Orchidaceae; wasp pollination; bee pollination; fly pollination; reproductive success; flower traits; scent; morphology; colour; sexual deception

Figure 1. The structure of an orchid, depicted using the European bee‐pollinated Ophrys dimidiata as a model. (a) Front view showing the tepals composed of the three large sepals, the two small petals and the third modified petal, the lip. The column consists of the pollinia and their associated structures and the stigmatic cavity. (b) Side view showing the pollinia, the viscidia and the stigma. (c) Ophrys dimidiata with two males pollinators, belonging to the longhorn bee Eucera dimidiata (Note: the pictures were taken during behavioural experiments, observing this phenomenon by chance is similar to winning the lottery.)
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References

Arditti J and Ghani AKA (2000) Tansley review no. 110. Numerical and physical properties of orchid seeds and their biological implications. New Phytologist 145: 367–421.

Ayasse M, Schiestl FP, Paulus HF, Ibarra F and Francke W (2003) Pollinator attraction in a sexually deceptive orchid by means of unconventional chemicals. Proceedings of the Royal Society of London B 270: 517–522.

Ayasse M (2006) Floral scent and pollinator attraction in sexually deceptive orchids. In: Dudareva N and Pichersky E (eds) Biology of Floral Scent. CRC Press: Boca Raton.

Ayasse M, Stökl J and Francke W (2011) Chemical ecology and pollinator‐driven speciation in sexually deceptive orchids. Phytochemistry 72 (13): 1667–1677.

Blanco MA and Barboza G (2005) Pseudocopulatory pollination in Lepanthes (Orchidaceae: Pleurothallidinae) by fungus gnats. Annals of Botany 95 (5): 763–772.

Bohman B, Phillips RD, Menz MH, et al. (2014) Discovery of pyrazines as pollinator sex pheromones and orchid semiochemicals: implications for the evolution of sexual deception. New Phytologist 203 (3): 939–952.

Breitkopf H, Onstein RE, Cafasso D, Schlüter PM and Cozzolino S (2015) Multiple shifts to different pollinators fueled rapid diversification in sexually deceptive Ophrys orchids. New Phytologist 207 (2): 377–389.

Chittka L and Raine NE (2006) Recognition of flowers by pollinators. Current Opinion in Plant Biology 9 (4): 428–435.

Cozzolino S and Widmer A (2005) Orchid diversity: an evolutionary consequence of deception? Trends in Ecology & Evolution 20 (9): 487–494.

Cuervo M, Rakosy D, Martel C, Schultz S and Ayasse M (2017) Sexual deception in the Eucera‐pollinated Ophrys leochroma: a chemical intermediate between wasp‐ and Andrena‐pollinated species. Journal of Chemical Ecology 43 (5): 469–479.

Ellis AG and Johnson SD (2010) Floral mimicry enhances pollen export: the evolution of pollination by sexual deceit outside of the Orchidaceae. The American Naturalist 176 (5): 143–151.

Gaskett AC and Herberstein ME (2010) Colour mimicry and sexual deception by tongue orchids (Cryptostylis). Naturwissenschaften 97 (1): 97.

Gaskett AC (2011) Orchid pollination by sexual deception: pollinator perspectives. Biological Reviews 86 (1): 33–75.

Gervasi DD, Selosse MA, Sauve M, et al. (2017) Floral scent and species divergence in a pair of sexually deceptive orchids. Ecology and Evolution 7 (15): 6023–6034.

Givnish TJ, Spalink D, Ames M, et al. (2015) Orchid phylogenomics and multiple drivers of their extraordinary diversification. Proceedings of the Royal Society B 282 (1814): 20151553.

Gögler J, Stökl J, Cortis P, et al. (2015) Increased divergence in floral morphology strongly reduces gene flow in sympatric sexually deceptive orchids with the same pollinator. Evolutionary Ecology 29 (5): 703–717.

Harari AR and Steinitz H (2013) The evolution of female sex pheromones. Current Zoology 59 (4): 569–578.

Hopper SD and Brown AP (2007) A revision of Australia's hammer orchids (Drakaea: Orchidaceae), with some field data on species‐specific sexually deceived wasp pollinators. Australian Systematic Botany 20 (3): 252–285.

de Jager ML and Peakall R (2015) Does morphology matter? An explicit assessment of floral morphology in sexual deception. Functional Ecology 30 (4): 537–546.

de Jager ML and Peakall R (2018) Experimental examination of pollinator‐mediated selection in a sexually deceptive orchid. Annals of Botany 123 (2): 347–354.

Kullenberg B (1961) Studies in Ophrys pollination. Zoologiska bidrag från Uppsala 34: 1–340.

Martel C, Cairampoma L, Stauffer FW and Ayasse M (2016) Telipogon peruvianus (Orchidaceae) flowers elicit pre‐mating behaviour in Eudejeania (Tachinidae) males for pollination. PLoS One 11 (11): e0165896.

Martel C, Francke W and Ayasse M (2019) The chemical and visual bases of the pollination of the Neotropical sexually deceptive orchid Telipogon peruvianus. New Phytologist 223 (4): 1989–2001.

Ne'eman G, Shavit O, Shaltiel L and Shmida A (2006) Foraging by male and female solitary bees with implications for pollination. Journal of Insect Behavior 19 (3): 383.

Osorio D and Vorobyev M (2008) A review of the evolution of animal colour vision and visual communication signals. Vision Research 48 (20): 2042–2051.

Paulus HF (2007) Wie Insekten‐Männchen von Orchideenblüten getäuscht werden – Bestäubungstricks und Evolution in der mediterranen Ragwurzgattung Ophrys. In: Gussenleitner F, Aubrecht G, Aescht E and Pfosser M (eds) Evolution – Phänomen Leben, vol. 20. Biologiezentrum der Oberösterreichischen Landesmuseen: Denisia.

Peakall R and Beattie AJ (1996) Ecological and genetic consequences of pollination by sexual deception in the orchid Caladenia tentactulata. Evolution 50 (6): 2207–2220.

Peakall R, Ebert D, Poldy J, et al. (2010) Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator‐driven speciation. New Phytologist 188 (2): 437–450.

Pridgeon AM, Cribb PJ and Chase MW (eds.) (1999) Genera Ochidacearum (Vol. 1). Oxford University Press: Oxford, UK.

Rakosy D, Streinzer M, Paulus HF and Spaethe J (2012) Floral visual signal increases reproductive success in a sexually deceptive orchid. Arthropod‐Plant Interactions 6 (4): 671–681.

Rakosy D, Cuervo M, Paulus HF and Ayasse M (2017) Looks matter: changes in flower form affect pollination effectiveness in a sexually deceptive orchid. Journal of Evolutionary Biology 30 (11): 1978–1993.

Schiestl FP, Ayasse M, Paulus HF, et al. (2000) Sex pheromone mimicry in the early spider orchid (Ophrys sphegodes): patterns of hydrocarbons as the key mechanism for pollination by sexual deception. Journal of Comparative Physiology A 186 (6): 567–574.

Schiestl FP and Ayasse M (2001) Post‐pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximising reproductive success? Oecologia 126 (4): 531–534.

Schiestl FP, Peakall R and Mant J (2004) Chemical communication in the sexually deceptive orchid genus Cryptostylis. Botanical Journal of the Linnean Society 144 (2): 199–205.

Schiestl FP and Cozzolino S (2008) Evolution of sexual mimicry in the orchid subtribe Orchidinae: the role of preadaptations in the attraction of male bees as pollinators. BMC Evolutionary Biology 8 (1): 27.

Schiestl FP and Schlüter PM (2009) Floral isolation, specialized pollination, and pollinator behavior in orchids. Annual Review of Entomology 54: 425–446.

Schiestl FP and Johnson SD (2013) Pollinator‐mediated evolution of floral signals. Trends in Ecology & Evolution 28 (5): 307–315.

Scopece G, Cozzolino S, Johnson SD and Schiestl FP (2010) Pollination efficiency and the evolution of specialized deceptive pollination systems. American Naturalist 175 (1): 98–105.

Singer RB (2002) The pollination mechanism in Trigonidium obtusum Lindl (Orchidaceae: Maxillariinae): sexual mimicry and trap‐flowers. Annals of Botany 89 (2): 157–163.

Singer RB, Flach A, Koehler S, Marsaioli AJ and Amaral MDCE (2004) Sexual mimicry in Mormolyca ringens (Lindl.) Schltr. (Orchidaceae: Maxillariinae). Annals of Botany 93 (6): 755–762.

Stejskal K, Streinzer M, Dyer A, Paulus HF and Spaethe J (2015) Functional significance of labellum pattern variation in a sexually deceptive orchid (Ophrys heldreichii): evidence of individual signature learning effects. PLoS One 10: e0142971.

Streinzer M, Paulus HF and Spaethe J (2009) Floral colour signal increases short‐range detectability of a sexually deceptive orchid to its bee pollinator. Journal of Experimental Biology 212 (9): 1365–1370.

Vereecken NJ and Schiestl FP (2008) The evolution of imperfect floral mimicry. Proceedings of the National Academy of Sciences of the United States of America 105 (21): 7484–7488.

Vereecken NJ and Schiestl FP (2009) On the roles of colour and scent in a specialized floral mimicry system. Annals of Botany 104 (6): 1077–1084.

Vereecken NJ, Wilson CA, Hötling S, et al. (2012) Pre‐adaptations and the evolution of pollination by sexual deception: Cope's rule of specialization revisited. Proceedings of the Royal Society B: Biological Sciences 279 (1748): 4786–4794.

Vereecken NJ and Francisco A (2014) Ophrys pollination: from Darwin to the present day. In: Edens‐Meier R and Bernhardt P (eds) Darwin's Orchids: Then and Now. The University of Chicago Press: Chicago.

Vignolini S, Davey MP, Bateman RZ, et al. (2012) The mirror crack'd: both pigment and structure contribute to the glossy blue appearance of the mirror orchid, Ophrys speculum. New Phytologist 196 (4): 1038–1047.

Watthana S, Kocyan A and Srimuang KO (2013) Pollination biology of Luisia curtisii (Orchidaceae): indications of a deceptive system operated by beetles. Plant Systematics and Evolution 299 (1): 177–185.

Weber A and Rakosy D (2013) The orchid flower. In: Rakosy D, Speckmaier M, Weber A, Huber W and Weissenhofer A (eds) Orchids – Botanical Jewels of the Golfo Dulce Region. Verein zur Förderung der Tropenstation La Gamba: Costa Rica; Wien, Austria.

Xu S, Schlueter PM, Scopece G, et al. (2011) Floral isolation is the main reproductive barrier among closely related sexually deceptive orchids. Evolution 65 (9): 2606–2620.

Further Reading

Bateman RM, Bradshaw E and Devey DS (2011) Species arguments: clarifying competing concepts of species delimitation in the pseudo‐copulatory orchid genus Ophrys. Botanical Journal of the Linnean Society 165 (4): 336–347.

Jersáková J, Johnson SD and Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biological Reviews 81 (2): 219–235.

Johnson SD and Schiestl FP (2016) Floral Mimicry. Oxford University Press: Oxford, UK.

Scopece G, Musacchio A, Widmer A and Cozzolino S (2007) Patterns of reproductive isolation in Mediterranean deceptive orchids. Evolution: International Journal of Organic Evolution 61 (11): 2623–2642.

Stashenko EE and Martínez JR (2008) Sampling flower scent for chromatographic analysis. Journal of Separation Science 31 (11): 2022–2031.

Tholl D and Röse US (2006) Detection and identification of floral scent compounds. In: Dudareva N and Pichersky E (eds) Biology of Floral Scent. CRC Press: Boca Raton.

Tremblay RL, Ackerman JD, Zimmerman JK and Calv RN (2004) Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnean Society 84 (1): 1–54.

Vereecken NJ (2009) Deceptive behavior in plants. I. Pollination by sexual deception in orchids: a host–parasite perspective. In: Baluska F Plant‐Environment Interactions. Springer‐Verlag: Berlin, Heidelberg.

Vereecken NJ, Streinzer M, Ayasse M, et al. (2011) Integrating past and present studies on Ophrys pollination – a comment on Bradshaw et al. Botanical Journal of the Linnean Society 165 (4): 329–335.

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Rakosy, Demetra(Mar 2020) Sexual Deception in Orchids. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028125]