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The orchid family is renowned for its enormous diversity of pollination mechanisms and unusually high occurrence of non-rewarding flowers compared to other plant families. The mechanisms of deception in orchids include generalized food deception, food-deceptive floral mimicry, brood-site imitation, shelter imitation, pseudoantagonism, rendezvous attraction and sexual deception. Generalized food deception is the most common mechanism (reported in 38 genera) followed by sexual deception (18 genera). Floral deception in orchids has been intensively studied since Darwin, but the evolution of non-rewarding flowers still presents a major puzzle for evolutionary biology. The two principal hypotheses as to how deception could increase fitness in plants are (i) reallocation of resources associated with reward production to flowering and seed production, and (ii) higher levels of cross-pollination due to pollinators visiting fewer flowers on non-rewarding plants, resulting in more outcrossed progeny and more efficient pollen export. Biologists have also tried to explain why deception is overrepresented in the orchid family. These explanations include: (i) efficient removal and deposition of pollinaria from orchid flowers in a single pollinator visit, thus obviating the need for rewards to entice multiple visits from pollinators; (ii) efficient transport of orchid pollen, thus requiring less reward-induced pollinator constancy; (iii) low-density populations in many orchids, thus limiting the learning of associations of floral phenotypes and rewards by pollinators; (iv) packaging of pollen in pollinaria with limited carry-over from flower to flower, thus increasing the risks of geitonogamous self-pollination when pollinators visit many flowers on rewarding plants. All of these general and orchid-specific hypotheses are difficult to reconcile with the well-established pattern for rewardlessness to result in low pollinator visitation rates and consequently low levels of fruit production. Arguments that deception evolves because rewards are costly are particularly problematic in that small amounts of nectar are unlikely to have a significant effect on the energy budget of orchids, and because reproduction in orchids is often severely pollen-, rather than resource-limited. Several recent experimental studies have shown that deception promotes cross-pollination, but it remains unknown whether actual outcrossing rates are generally higher in deceptive orchids. Our review of the literature shows that there is currently no evidence that deceptive orchids carry higher levels of genetic load (an indirect measure of outcrossing rate) than their rewarding counterparts. Cross-pollination does, however, result in dramatic increases in seed quality in almost all orchids and has the potential to increase pollen export (by reducing pollen discounting). We suggest that floral deception is particularly beneficial, because of its promotion of outcrossing, when pollinators are abundant, but that when pollinators are consistently rare, selection ...

SummaryAlthough not 'a professed botanist', Charles Darwin made seminal contributions to understanding of floral and inflorescence function while seeking evidence of adaptation by natural selection. This review considers the legacy of Darwin's ideas from three perspectives. First, we examine the process of floral and inflorescence adaptation by surveying studies of phenotypic selection, heritability and selection responses. Despite widespread phenotypic and genetic capacity for natural selection, only one-third of estimates indicate phenotypic selection. Second, we evaluate experimental studies of floral and inflorescence function and find that they usually demonstrate that reproductive traits represent adaptations. Finally, we consider the role of adaptation in floral diversification. Despite different diversification modes (coevolution, divergent use of the same pollen vector, pollinator shifts), evidence of pollination ecotypes and phylogenetic patterns suggests that adaptation commonly contributes to floral diversity. Thus, this review reveals a contrast between the inconsistent occurrence of phenotypic selection and convincing experimental and comparative evidence that floral traits are adaptations. Rather than rejecting Darwin's hypotheses about floral evolution, this contrast suggests that the tempo of creative selection varies, with strong, consistent selection during episodes of diversification, but relatively weak and inconsistent selection during longer, 'normal' periods of relative phenotypic stasis. I. Introduction'During the summer of 1839 ... I was led to attend to the crossfertilisation of flowers by the aid of insects, from having come to the conclusion in my speculations on the origin of species, that crossing played an important part in keeping specific forms constant. I attended to the subject more or less during every subsequent summer ... ' Darwin (1887, p. 90 Review 531A celebration of Darwin's contributions would be incomplete without consideration of pollination and floral adaptation. The preceding quotation illustrates that Darwin actively examined this subject after age 30 yr and it highlights two of his central themes: adaptation by natural selection and the benefits of outcrossing. Darwin introduced these themes, as illustrated by plant reproduction, in The Origin of Species (Darwin, 1859) and elaborated on them in books on orchid pollination (Darwin, 1862, 1877a: Fig. 1), cross-fertilization and self-fertilization (Darwin, 1876), and heterostyly and dioecy (Darwin, 1877b). His detailed interpretations of orchid flowers as outcrossing adaptations specifically inspired the golden age of pollination biology during the late nineteenth century and, together with his general evolutionary insights, laid the foundation for current understanding of floral function. Indeed, Darwin's perspectives on floral function continue to motivate studies of plant reproduction and some of his hypotheses have been tested only recently (Table 1).Darwin considered floral traits as 'beautiful contrivances'...

It has been debated whether pollination success in nonrewarding plants that flower in association with nectar‐producing plants will be diminished by competition for pollinator visits or, alternatively, enhanced through increased local abundance of pollinators (the magnet species effect). We experimentally evaluated these effects using the nonrewarding bumblebee‐pollinated orchid Anacamptis morio and associated nectar‐producing plants at a site in Sweden. Pollination success (estimated as pollen receipt and pollen removal) in A. morio was significantly greater for individuals translocated to patches of nectar‐producing plants (Geum rivale and Allium schoenoprasum) than for individuals placed outside (∼20 m away) such patches. These results provide support for the existence of a facilitative magnet species effect in the interaction between certain nectar plants and A. morio. To determine the spatial scale of these interactions, we correlated the visitation rate to flowers of A. morio with the density of sympatric nectar plants in 1‐m2 and 100‐m2 plots centered around groups of translocated plants, and at the level of whole meadows (∼0.5–2 ha). Visitation rate to flowers of A. morio was not correlated with the 1‐m2 patch density of G. rivale and A. schoenoprasum, but showed a significant positive relationship with density of these nectar plants in 100‐m2 plots. In addition, visitation to flowers of A. morio was strongly and positively related to the density of A. schoenoprasum at the level of the meadow. Choice experiments showed that bees foraging on the purple flowers of A. schoenoprasum (a particularly effective magnet species) visit the purple flowers of A. morio more readily (47.6% of choices) than bees foraging on the yellow flowers of Lotus corniculatus (17% of choices). Overall similarity in flower color and shape may increase the probability that a pollinator will temporarily shift from a nectar‐producing “magnet” plant to a nonrewarding plant. We discuss the possibility of a mimicry continuum between those orchids that exploit instinctive food‐seeking behavior of pollinators and those that show an adaptive resemblance to nectar‐producing plants.