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Deception has evolved in a range of taxa. When deception imposes costs, yet persists over generations, exploited species typically have traits to help them bear or minimise costs. The sexually deceptive orchids, Cryptostylis spp., are pollinated by tricking male haplodiploid wasps (Lissopimpla excelsa) into mating with flowers, which offer no reward and often elicit sperm wastage. We hypothesise that by attracting haplodiploid species, orchids have a pollinator ideally suited to withstand the costs of sexual deception-and a selective advantage compared to other orchids. Haplodiploid females can reproduce with or without sperm-albeit when spermless, females can only have sons. Through orchid deception and sperm wastage, deceived haplodiploid populations could become male biased, providing enough males to share between orchids and females. In this way, pollinator populations can persist despite high densities of sexually deceptive orchids. Here, we aim to broadly test this prediction using museum and digital records of the pollinator, L. excelsa, from sites with or without orchids. For robustness, we also analyse the sex ratio of a sister ichneumonid species that occurs in the same areas but is not deceived by orchids. We found that at sites with orchids, L. excelsa was significantly more male biased than at sites without orchids and significantly more male biased than the sister ichneumonid. This survey is the first to test the population-level effects of sexually deceptive orchids on their pollinator. It supports our prediction that orchid deception can drive male-biased sex ratios in exploited pollinators.

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 coevolution or an arms race between orchids and their pollinators. Botanists, taxonomists and chemical ecologists have made remarkable progress in the study of deceptive orchid pollination. Further complementary investigations from entomology and behavioural ecology perspectives should prove fascinating and engender a more complete understanding of the evolution and maintenance of such enigmatic plant-animal interactions., (© 2010 The Author. Biological Reviews © 2010 Cambridge Philosophical Society.)

Typically, floral colour attracts pollinators by advertising rewards such as nectar, but how does colour function when pollinators are deceived, unrewarded, and may even suffer fitness costs? Sexually deceptive orchids are pollinated only by male insects fooled into mating with orchid flowers and inadvertently transferring orchid pollinia. Over long distances, sexually deceptive orchids lure pollinators with counterfeit insect sex pheromones, but close-range deception with colour mimicry is a tantalising possibility. Here, for the first time, we analyse the colours of four sexually deceptive Cryptostylis orchid species and the female wasp they mimic (Lissopimpla excelsa, Ichneumonidae), from the perspective of the orchids' single, shared pollinator, male Lissopimpla excelsa. Despite appearing different to humans, the colours of the orchids and female wasps were effectively identical when mapped into a hymenopteran hexagonal colour space. The orchids and wasps reflected predominantly red-orange wavelengths, but UV was also reflected by raised bumps on two orchid species and by female wasp wings. The orchids' bright yellow pollinia contrasted significantly with their overall red colour. Orchid deception may therefore involve accurate and species-specific mimicry of wavelengths reflected by female wasps, and potentially, exploitation of insects' innate attraction to UV and yellow wavelengths. In general, mimicry may be facilitated by exploiting visual vulnerabilities and evolve more readily at the peripheries of sensory perception. Many sexually deceptive orchids are predominantly red, green or white: colours that are all potentially difficult for hymenoptera to detect or distinguish from the background.

Floral traits such as odor, color, and morphology are important pollinator attractants. Variation in floral traits may influence floral constancy, the tendency of pollinating insects to visit flowers of only one type. We investigated for the first time variation in odor between floral morphs in heterostylous species. We analyzed inter- and intraspecific odor variation in the "pin" and "thrum" floral morphs of sympatric Primula elatior and P. farinosa (Primulaceae). Floral volatiles were sampled with headspace sorption. Quantitative analysis and chemical identification were performed by gas chromatography coupled to mass spectrometry. The species produced different floral bouquets. P. elatior emitted mostly limonene with small amounts of alpha-pinene, myrcene, and sabinene. P. farinosa produced benzaldehyde, 4-oxoisophorone (2,6,6-trimethyl-2-cyclohexene-1,4-dione), benzyl alcohol, and benzyl acetate. These interspecific differences may play a role in promoting floral constancy and maintaining species integrity. Conversely, no differences were detected between the scents of pin and thrum morphs within each species. Heterostyly relies on pollinators visiting both floral morphs. There may be stabilizing selection against divergences in traits that may cause pollinators to develop floral constancy to only one of the floral morphs.