Evolution of honest reward signal in flowers

Some flowering plants signal the abundance of their rewards by changing their flower colour, scent or other floral traits as rewards are depleted. These floral trait changes can be regarded as honest signals of reward states for pollinators. Previous studies have hypothesized that these signals are used to maintain plant-level attractiveness to pollinators, but the evolutionary conditions leading to the development of honest signals have not been well investigated from a theoretical basis. We examined conditions leading to the evolution of honest reward signals in flowers by applying a theoretical model that included pollinator response and signal accuracy. We assumed that pollinators learn floral traits and plant locations in association with reward states and use this information to decide which flowers to visit. While manipulating the level of associative learning, we investigated optimal flower longevity, the proportion of reward and rewardless flowers, and honest- and dishonest-signalling strategies. We found that honest signals are evolutionarily stable only when flowers are visited by pollinators with both high and low learning abilities. These findings imply that behavioural variation in learning within a pollinator community can lead to the evolution of an honest signal even when there is no contribution of rewardless flowers to pollinator attractiveness.

Noisy communities and signal detection: why do foragers visit rewardless flowers?

Floral communities present complex and shifting resource landscapes for flower-foraging animals. Strong similarities among the floral displays of different plant species, paired with high variability in reward distributions across time and space, can weaken correlations between floral signals and reward status. As a result, it should be difficult for foragers to discriminate between rewarding and rewardless flowers. Building on signal detection theory in behavioural ecology, we use hypothetical probability density functions to examine graphically how plant signals pose challenges to forager decision-making. We argue that foraging costs associated with incorrect acceptance of rewardless flowers and incorrect rejection of rewarding ones interact with community-level reward availability to determine the extent to which rewardless and rewarding species should overlap in flowering time. We discuss the evolutionary consequences of these phenomena from both the forager and the plant perspectives. This article is part of the theme issue ‘Signal detection theory in recognition systems: from evolving models to experimental tests’.

Evidence for a food-deceptive pollination system using Hylaeus bees in Caladenia hildae (Orchidaceae)

Numerous orchid species are pollinated by food deception, where rewardless flowers attract foraging pollinators through the mimicry of other flowers or the use of non-specific floral signals. Here we investigate the pollination of Caladenia hildae, a member of a diverse Australian genus containing species pollinated by sexual deception, and species pollinated by food foraging pollinators. Despite eight bee species occurring at the main study site, only food foraging bees of a single species of Hylaeus (Colletidae) were observed to remove and deposit pollen of C. hildae. Spectral reflectance of C. hildae flowers differed from co-flowering rewarding species in terms of both the wavelengths of light reflected, and the pattern of colouration. As such, there was no evidence that C. hildae uses a pollination strategy based on floral mimicry. However, the attraction of only a single bee species at this site suggests that C. hildae may use a deceptive strategy that exploits sensory biases or behaviours that differ between Hylaeus sp. and the remainder of the bee community. While Hylaeus have been recorded visiting orchid flowers in several parts of the world, C. hildae may represent the first documented case of an orchid species specialised on pollination by Hylaeus bees.

Recent advances on evolution of pollination systems and reproductive biology of Vanilloideae (Orchidaceae)

Vanilloideae as currently circumscribed comprises nine genera and two tribes: Vanilleae and Pogonieae. The pantropical genus Vanilla has been frequently assumed to be natural on the basis of its climbing habit and lateral inflorescences. However, the inclusion of the rare Dictyophyllaria dietschiana in phylogenetic analyses makes the genus Vanilla paraphyletic. Within Pogonieae, phylogenetic analyses show that inclusion of Pogoniopsis turns the tribe paraphyletic. All analyses reveal that Pogoniopsis is closely related to members of Epidendroideae. Members of Pogonieae are pollinated by several groups of solitary and social bees, two pollination systems being recognized: reward-producing and deceptive. Molecular phylogeny suggests that the common ancestor to Pogonieae gave rise to two evolutionary lineages: one tropical with a condition of reward production; and one predominantly temperate-invading line with deceptive flowers. Reward-producing flowers characterize South and Central American clade (= Cleistes), while deceptive pollination is prominent in the clade including North American-Asiatic taxa plus Amazonian Duckeella. Species of “orchid bees” have been recorded as pollinators of the genus Vanilla (V. planifolia group and V. pompona group) in the Neotropics. In species of the V. pompona group, these bees are attracted by the fragrance of the flowers. Hummingbirds have been reported to pollinate some species of Vanilla. Vanilla insignis, V. odorata and V. planifolia are known to be pollinated through generalized food deception. Some species of Vanilla yield fruits through spontaneous self-pollination. This form of autogamy has been reported for V. griffithii, V. palmarum, V. planifolia, V. savannarum and V. bicolor. In Brazil, data on the pollination biology of Vanilla are scarce, but conclusive data are available for V. edwallii, which is pollinated by Epicharis (Apidae: Centridini). This species is rewardless, but male Epicharis are attracted to its flowers by their fragrance. Additionally, the Brazilian V. dubia and E. sclerophyllum are pollinated by bees. The mentum region of V. dubia and V. edwallii is dry, whereas that of E. sclerophyllum presents a small quantity of nectar. Flowers of E. sclerophyllum are scentless, while those of V. dubia are odoriferous. Vanilla dubia and V. edwallii are self-compatible and need a pollinator to yield fruits. In contrast, Epistephium sclerophyllum sets fruits through spontaneous self-pollination, but biotic pollination also occurs. Both species are primarily adapted to pollination by euglossine bees. Pollination by Euglossini seems to have evolved at least twice along the evolution of Vanilleae. Furthermore, shifts between rewarding and rewardless flowers and between autogamous and allogamous species have been reported among vanillas.