No abstract
Pollinator-driven diversification is thought to be a major source of floral variation in plants. Our knowledge of this process is, however, limited to indirect assessments of evolutionary changes. Here, we employ experimental evolution with fast cycling Brassica rapa plants to demonstrate adaptive evolution driven by different pollinators. Our study shows pollinator-driven divergent selection as well as divergent evolution in plant traits. Plants pollinated by bumblebees evolved taller size and more fragrant flowers with increased ultraviolet reflection. Bumblebees preferred bumblebee-pollinated plants over hoverfly-pollinated plants at the end of the experiment, showing that plants had adapted to the bumblebees' preferences. Plants with hoverfly pollination became shorter, had reduced emission of some floral volatiles, but increased fitness through augmented autonomous self-pollination. Our study demonstrates that changes in pollinator communities can have rapid consequences on the evolution of plant traits and mating system.
Summary Sexually deceptive orchids are predicted to represent a special case of plant speciation where strong reproductive isolation may be achieved by differences in floral scent. In this study of Australian sexually deceptive Chiloglottis orchids, we performed choice experiments to test for wasp pollinator specificity in the field; identified the compounds involved in pollinator attraction by gas chromatography with electroantennographic detection (GC‐EAD), gas chromatography with mass selective detection (GC‐MS), chemical synthesis and behavioural bioassays; and mapped our chemical findings on to a phylogeny of the orchids. Field experiments confirmed pollination is a highly specific interaction, but also revealed a pool of nonpollinating ‘minor responder’ wasps. Six novel compounds, all 2,5‐dialkylcyclohexan‐1,3‐diones, called ‘chiloglottones’, were discovered to be involved in pollinator attraction. Bioassays confirmed that pollinator specificity has a strong chemical basis, with specificity among sympatric orchids maintained by either different single compounds or a variation in a blend of two compounds. The phylogenetic overlay confirmed that speciation is always associated with pollinator switching and usually underpinned by chemical change. If the chemical differences that control reproductive isolation in Chiloglottis have a strong genetic basis, and given the confirmed pool of potential pollinators, we conclude that pollinator‐driven speciation appears highly plausible in this system.
The "sexually deceptive" orchid Chiloglottis trapeziformis attracts males of its pollinator species, the thynnine wasp Neozeleboria cryptoides, by emitting a unique volatile compound, 2-ethyl-5-propylcyclohexan-1,3-dione, which is also produced by female wasps as a male-attracting sex pheromone.
A standing enigma in pollination ecology is the evolution of pollinator attraction without offering reward in about one third of all orchid species. Here I review concepts of pollination by deception, and in particular recent findings in the pollination syndromes of food deception and sexual deception in orchids. Deceptive orchids mimic floral signals of rewarding plants (food deception) or mating signals of receptive females (sexual deception) to attract pollen vectors. In some food deceptive orchids, similarities in the spectral reflectance visible to the pollinator in a model plant and its mimic, and increased reproductive success of the mimic in the presence of the model have been demonstrated. Other species do not mimic specific model plants but attract pollinators with general attractive floral signals. In sexually deceptive orchids, floral odor is the key trait for pollinator attraction, and behaviorally active compounds in the orchids are identical to the sex pheromone of the pollinator species. Deceptive orchids often show high variability in floral signals, which may be maintained by negative frequency-dependent selection, since pollinators can learn and subsequently avoid common deceptive morphs more quickly than rare ones. The evolution of obligate deception in orchids seems paradoxical in the light of the typically lower fruit set than in rewarding species. Pollination by deception, however, can reduce self-pollination and encourage pollen flow over longer distances, thus promoting outbreeding. Although some food deceptive orchids are isolated through postzygotic reproductive barriers, sexually deceptive orchids lack post-mating barriers and species isolation is achieved via specific pollinator attraction. Recent population genetic and phylogenetic investigations suggest gene-flow within subgeneric clades, but pollinator-mediated selection may maintain species-specific floral traits.
Recent studies have suggested that bacterial volatiles play an important role in bacterial-plant interactions. However, few reports of bacterial species that produce plant growth modulating volatiles have been published, raising the question whether this is just an anecdotal phenomenon. To address this question, we performed a large screen of strains originating from the soil for volatile-mediated effects on Arabidopsis thaliana. All of the 42 strains tested showed significant volatile-mediated plant growth modulation, with effects ranging from plant death to a sixfold increase in plant biomass. The effects of bacterial volatiles were highly dependent on the cultivation medium and the inoculum quantity. GC-MS analysis of the tested strains revealed over 130 bacterial volatile compounds. Indole, 1-hexanol and pentadecane were selected for further studies because they appeared to promote plant growth. None of these compounds triggered a typical defence response, using production of ethylene and of reactive oxygen species (ROS) as read-outs. However, when plants were challenged with the flg-22 epitope of bacterial flagellin, a prototypical elicitor of defence responses, additional exposure to the volatiles reduced the flg-22-induced production of ethylene and ROS in a dose-dependent manner, suggesting that bacterial volatiles may act as effectors to inhibit the plant's defence response.
Plants have evolved a range of strategies to manipulate the behaviour of their insect partners. One powerful strategy is to produce signals that already have a role in the animalsÕ own communication systems. To investigate to what extent the evolution of floral scents is correlated with chemical communication in insects, I analyse the occurrence, commonness, and evolutionary patterns of the 71 most common ÔfloralÕ volatile organic compounds (VOCs) in 96 plant families and 87 insect families. I found an overlap of 87% in VOCs produced by plants and insects. ÔFloralÕ monoterpenes showed strong positive correlation in commonness between plants (both gymnosperms and angiosperms) and herbivores, whereas the commonness of ÔfloralÕ aromatics was positively correlated between angiosperms and both pollinators and herbivores. According to a multivariate regression analysis the commonness of ÔfloralÕ aromatics was best explained by their commonness in pollinators, whereas monoterpenes were best explained by herbivores. Among pollinator orders, aromatics were significantly more common in Lepidoptera than in Hymenoptera, whereas monoterpenes showed no difference among the two orders. Collectively, these patterns suggest that plants and insects converge in overall patterns of volatile production, both for attraction and defence. Monoterpenes seem to have evolved primarily for defence under selection by herbivores, whereas aromatics evolved signalling functions in angiosperms, primarily for pollinator attraction.
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