Mechanisms and evolution of deceptive pollination in orchids

Abstract

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 ...

A new vanilla species from Costa Rica closely related to V. planifolia (Orchidaceae)

“…nov. compared to V. planifolia may also contribute to favor self or geitonogamous pollination as well as provide greater reproductive success to V. sotoarenasii sp. nov., as pointed out for non-rewarding orchids (Jersáková et al 2006;Sun et al 2009). …”

Sensory Exploitation: Underestimated in the Evolution of Art As Once in Sexual Selection Theory?

“…For instance, in the genus Ophrys, plants evolved to attract male bees as pollinators by mimicking female mating signals. Here evolution by SE -the plants don't give any rewards in return -seems to be the only possible explanation (Schiestl and Cozzolino 2008;Jersakova et al 2006). Of course, in this example indirect benefits don't apply because sensory biases of another species are exploited.…”

Variable responses of hawkmoths to nectar-depleted plants in two native Petunia axillaris (Solanaceae) populations

“…Nevertheless most angiosperms produce a nectar reward for pollinators, while well-studied cases like deceptive orchids are the exception (Duffy and Stout 2008;Gigord et al 2002Gigord et al , 2004Internicola et al 2006;Sun et al 2010). The persistence of deceptive orchids demonstrates that cheating can be an evolutionarily stable strategy under certain circumstances (Jersakova et al 2006;Maynard-Smith 1982).…”