The mating consequences of rewarding vs. deceptive pollination systems: Is there a quantity–quality trade‐off?

Abstract Plant mating commonly involves quality–quantity trade‐offs. Such a trade‐off features explicitly in the cross‐promotion hypothesis for the evolution of pollination by deceit. According to this hypothesis, rewardlessness enhances mating quality by altering pollinator behavior in ways that reduce self‐pollination and increase outcrossing, thus compensating for the reduced pollen dispersal and seed production resulting from lack of reinforcement of pollinator visitation behavior. The high prevalence of rewardlessness in orchids suggests that deceit pollination conveys benefits that outweigh the fecundity advantages of reward production. We test the cross‐promotion hypothesis in Disa, an African orchid genus in which nectar rewards have evolved repeatedly from rewardless ancestors. To address this hypothesis directly, we quantified pollinator behavior and the associated dispersal of stained pollen for four nectar‐producing (N+) and 10 nectarless (N−) species. We also assessed more extensive, if less direct, evidence from a survey of lifetime pollination outcomes for 15 N+ and 32 N− species. Pollinators visited N+ species more frequently and visited 1.5 times more flowers per inflorescence than in N− species. In contrast, pollinators skipped more conspecific plants between visits to donor and recipient plants when visiting N− species than when visiting N+ species. Over floral lifetimes, both N− and N+ species exhibited similar overall pollen‐transfer efficiency (8.2%) and did not differ in the overall fractions of pollen involved in self‐pollination (26% of all pollen deposited), geitonogamy (82% of all self‐pollination), or export to other conspecific plants (74%). N+ species set more fruit per flower (68.8% vs. 48.8%), but equivalent fractions of ovules per fruit were fertilized and subsequently developed into seeds in N− and N+ species. These findings provide only limited evidence that deceit pollination enhances mating quality (nectar production causes more local mating in N+ species than in N− species). Contrary to the hypothesis, deceit does not generally affect pollinator‐mediated self‐pollination. The repeated evolution of nectar production from rewardless ancestors in Disa likely occurred under severe visit limitation, favoring nectar‐producing mutants with higher reproductive output. Given that we did not find any mating quality advantage for rewardlessness in Disa, its persistence in some lineages remains an evolutionary enigma.

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