Orchid pollination by sexual deception: pollinator perspectives

Abstract

The extraordinary taxonomic and morphological diversity of orchids is accompanied by a remarkable range of pollinators and pollination systems. Sexually deceptive orchids are adapted to attract specific male insects that are fooled into attempting to mate with orchid flowers and inadvertently acting as pollinators. This review summarises current knowledge, explores new hypotheses in the literature, and introduces some new approaches to understanding sexual deception from the perspective of the duped pollinator. Four main topics are addressed: (1) global patterns in sexual deception, (2) pollinator identities, mating systems and behaviours, (3) pollinator perception of orchid deceptive signals, and (4) the evolutionary implications of pollinator responses to orchid deception, including potential costs imposed on pollinators by orchids. A global list of known and putative sexually deceptive orchids and their pollinators is provided and methods for incorporating pollinator perspectives into sexual deception research are provided and reviewed. At present, almost all known sexually deceptive orchid taxa are from Australia or Europe. A few sexually deceptive species and genera are reported for New Zealand and South Africa. In Central and Southern America, Asia, and the Pacific many more species are likely to be identified in the future. Despite the great diversity of sexually deceptive orchid genera in Australia, pollination rates reported in the literature are similar between Australian and European species. The typical pollinator of a sexually deceptive orchid is a male insect of a species that is polygynous, monandrous, haplodiploid, and solitary rather than social. Insect behaviours involved in the pollination of sexually deceptive orchids include pre-copulatory gripping of flowers, brief entrapment, mating, and very rarely, ejaculation. Pollinator behaviour varies within and among pollinator species. Deception involving orchid mimicry of insect scent signals is becoming well understood for some species, but visual and tactile signals such as colour, shape, and texture remain neglected. Experimental manipulations that test for function, multi-signal interactions, and pollinator perception of these signals are required. Furthermore, other forms of deception such as exploitation of pollinator sensory biases or mating preferences merit more comprehensive investigation. Application of molecular techniques adapted from model plants and animals is likely to deliver new insights into orchid signalling, and pollinator perception and behaviour. There is little current evidence that sexual deception drives any species-level selection on pollinators. Pollinators do learn to avoid deceptive orchids and their locations, but this is not necessarily a response specific to orchids. Even in systems where evidence suggests that orchids do interfere with pollinator mating opportunities, considerable further research is required to determine whether this is sufficient to impose selection on pollinators or generate antagonistic coevolu...

Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species

“…Numerous studies have shown that these color patterns are critically important for plant-pollinator interactions (1)(2)(3)(4)(5)(6)(7)(8). Among the most captivating examples are deceptive orchids that display floral pigment patterns remarkably similar to female bees or wasps to lure male counterparts for pseudocopulation, thereby achieving pollination (9)(10)(11).…”

Floral scent and species divergence in a pair of sexually deceptive orchids

“…Sexual deception, currently known in several genera of orchids, and one genus of Asteraceae and Iridaceae, respectively, is a highly specific pollination mechanism (Gaskett, 2011; Johnson & Schiestl, 2016). Sexually deceptive plants mimic mating signals of their pollinators, such as sex pheromones, morphology, and surface pilosity, and entice their pollinators into attempted copulations with their flowers (Peakall & Whitehead, 2014; Peakall et al., 2010; Schiestl & Schlüter, 2009; Schiestl et al., 1999).…”

Pollinator sharing by the sexually deceptive Green-comb Spider Orchids, Caladenia phaeoclavia, C. parva and C. villosissima (Orchidaceae: Caladeniinae): taxonomic considerations

“…Experimental evidence for pollinator specificity in sexually By contrast to the lack of pollinator sharing in Chiloglottis and Drakaea revealed by field choice testing, published pollinator lists suggest pollinator sharing may occur in some groups of sexually deceptive, Thynnid-pollinated Caladenia species in eastern Australia (Phillips et al 2009, Gaskett 2010. While most sexually deceptive Caladenia species attract unique pollinators, nine species in the Caladenia reticulata complex are pollinated by Phymatothynnus near nitidus 1, three species of Greencomb Spider Orchids are pollinated by Lophocheilus anilitatus and Caladenia tesselata shares P. near nitidus 1 with the C. reticulata group (Phillips et al 2009, Gaskett 2010. These data contrast markedly with results for Chiloglottis and Drakaea, and suggest that factors other than pollinator specificity may govern reproductive isolation in some Caladenia clades.…”

“…Pollination by sexual deception of male insects has evolved independently in multiple lineages of the Orchidaceae principally on two continents, Europe and Australia, and involves hundreds of species (Gaskett 2010). Pollen transfer occurs in sexually deceptive orchids when female mimicking labellum structures stimulate mating behaviours in deceived males Francisco 2014, Bower 2014).…”

“…Overall, the sharing of the same vector species among ten reticulata complex species combined with evidence of very low genetic divergence suggested they belong to the same biological species and most likely represent an example of taxonomic over-splitting (Swartz et al 2014). This paper uses pollinator baiting and controlled field choice tests to examine putative pollinator sharing (Phillips et al 2009, Gaskett 2010 across the geographical distributions of three closely similar, sexually deceptive species of Greencomb Spider Orchids; Caladenia parva G.W. Carr, C. phaeoclavia D.L.…”