Biological communication by means of structural color has existed for at least 500 million years. Structural color is commonly observed in the animal kingdom, but has been little studied in plants. We present a striking example of multilayer-based strong iridescent coloration in plants, in the fruit of Pollia condensata. The color is caused by Bragg reflection of helicoidally stacked cellulose microfibrils that form multilayers in the cell walls of the epicarp. We demonstrate that animals and plants have convergently evolved multilayer-based photonic structures to generate colors using entirely distinct materials. The bright blue coloration of this fruit is more intense than that of any previously described biological material. Uniquely in nature, the reflected color differs from cell to cell, as the layer thicknesses in the multilayer stack vary, giving the fruit a striking pixelated or pointillist appearance. Because the multilayers form with both helicoidicities, optical characterization reveals that the reflected light from every epidermal cell is polarized circularly either to the left or to the right, a feature that has never previously been observed in a single tissue.

Diverse forms of nanoscale architecture generate structural colour and perform signalling functions within and between species. Structural colour is the result of the interference of light from approximately regular periodic structures; some structural disorder is, however, inevitable in biological organisms. Is this disorder functional and subject to evolutionary selection, or is it simply an unavoidable outcome of biological developmental processes? Here we show that disordered nanostructures enable flowers to produce visual signals that are salient to bees. These disordered nanostructures (identified in most major lineages of angiosperms) have distinct anatomies but convergent optical properties; they all produce angle-dependent scattered light, predominantly at short wavelengths (ultraviolet and blue). We manufactured artificial flowers with nanoscale structures that possessed tailored levels of disorder in order to investigate how foraging bumblebees respond to this optical effect. We conclude that floral nanostructures have evolved, on multiple independent occasions, an effective degree of relative spatial disorder that generates a photonic signature that is highly salient to insect pollinators.

Plant volatiles play important roles in attraction of certain pollinators and in host location by herbivorous insects. Virus infection induces changes in plant volatile emission profiles, and this can make plants more attractive to insect herbivores, such as aphids, that act as viral vectors. However, it is unknown if virus-induced alterations in volatile production affect plant-pollinator interactions. We found that volatiles emitted by cucumber mosaic virus (CMV)-infected tomato (Solanum lycopersicum) and Arabidopsis thaliana plants altered the foraging behaviour of bumblebees (Bombus terrestris). Virus-induced quantitative and qualitative changes in blends of volatile organic compounds emitted by tomato plants were identified by gas chromatography-coupled mass spectrometry. Experiments with a CMV mutant unable to express the 2b RNA silencing suppressor protein and with Arabidopsis silencing mutants implicate microRNAs in regulating emission of pollinator-perceivable volatiles. In tomato, CMV infection made plants emit volatiles attractive to bumblebees. Bumblebees pollinate tomato by ‘buzzing’ (sonicating) the flowers, which releases pollen and enhances self-fertilization and seed production as well as pollen export. Without buzz-pollination, CMV infection decreased seed yield, but when flowers of mock-inoculated and CMV-infected plants were buzz-pollinated, the increased seed yield for CMV-infected plants was similar to that for mock-inoculated plants. Increased pollinator preference can potentially increase plant reproductive success in two ways: i) as female parents, by increasing the probability that ovules are fertilized; ii) as male parents, by increasing pollen export. Mathematical modeling suggested that over a wide range of conditions in the wild, these increases to the number of offspring of infected susceptible plants resulting from increased pollinator preference could outweigh underlying strong selection pressures favoring pathogen resistance, allowing genes for disease susceptibility to persist in plant populations. We speculate that enhanced pollinator service for infected individuals in wild plant populations might provide mutual benefits to the virus and its susceptible hosts.

SummaryIridescence is a form of structural coloration, produced by a range of structures, in which hue is dependent on viewing angle [1, 2, 3, 4]. One of these structures, the diffraction grating, is found both in animals (for example, beetles [2]) and in plants (on the petals of some animal pollinated flowers [5]). The behavioral impacts of floral iridescence and its potential ecological significance are unknown [6, 7, 8, 9]. Animal-pollinated flowers are described as “sensory billboards” [10], with many floral features contributing to a conspicuous display that filters prospective pollinators. Yet floral iridescence is more subtle to the human eye than that of many animal displays because the floral diffraction grating is not perfectly regular [5, 6, 7, 8, 9]. This presents a puzzle: if the function of petals is to attract pollinators, then flowers might be expected to optimize iridescence to increase showiness. On the other hand, pollinators memorize floral colors as consistent advertisements of reward quality, and iridescence might corrupt flower color identity. Here we tested the trade-off between flower detectability and recognition, requiring bumblebees (Bombus terrestris) to identify artificial flowers that varied in pigmentation and degree of iridescence. We find that iridescence does increase target detectability but that “perfect” iridescence (produced by an artificial diffraction grating) corrupts target identity and bees make many mistakes. However, “imperfect” floral iridescence does not lead to mistaken target identity, while still benefitting flower detectability. We hypothesize that similar trade-offs might be found in the many naturally “imperfect” iridescence-producing structures found in animal-animal, as well as other plant-animal, interactions.

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