More than 87% of flowering plant species are animal-pollinated [1] and produce floral scents and other signals to attract pollinators. These floral cues may however also attract antagonistic visitors, including herbivores [2]. The dilemma is exacerbated when adult insects pollinate the same plant that their larvae consume. It remains largely unclear how plants maximize their fitness under these circumstances. Here we show that in the night-flowering wild tobacco Nicotiana attenuata, the emission of a sesquiterpene, (E)-α-bergamotene, in flowers increases adult Manduca sexta moth-mediated pollination success, while the same compound in leaves is known to mediate indirect defense against M. sexta larvae [3, 4]. Forward and reverse genetic analyses demonstrated that both herbivory-induced and floral (E)-α-bergamotene are regulated by the expression of a monoterpene-synthase-derived sesquiterpene synthase (NaTPS38). The expression pattern of NaTPS38 also accounts for variation in (E)-α-bergamotene emission among natural accessions. These results highlight that differential expression of a single gene that results in tissue-specific emission of one compound contributes to resolving the dilemma for plants when their pollinators are also herbivores. Furthermore, this study provides genetic evidence that pollinators and herbivores interactively shape the evolution of floral signals and plant defense.

The hawkmoth Manduca sexta and one of its preferred hosts in the North American Southwest, Datura wrightii, share a model insect–plant relationship based on mutualistic and antagonistic life-history traits. D. wrightii is the innately preferred nectar source and oviposition host for M. sexta. Hence, the hawkmoth is an important pollinator while the M. sexta larvae are specialized herbivores of the plant. Olfactory detection of plant volatiles plays a crucial role in the behavior of the hawkmoth. In vivo, the odorant receptor coreceptor (Orco) is an obligatory component for the function of odorant receptors (ORs), a major receptor family involved in insect olfaction. We used CRISPR-Cas9 targeted mutagenesis to knock out (KO) the MsexOrco gene to test the consequences of a loss of OR-mediated olfaction in an insect–plant relationship. Neurophysiological characterization revealed severely reduced antennal and antennal lobe responses to representative odorants emitted by D. wrightii. In a wind-tunnel setting with a flowering plant, Orco KO hawkmoths showed disrupted flight orientation and an ablated proboscis extension response to the natural stimulus. The Orco KO gravid female displayed reduced attraction toward a nonflowering plant. However, more than half of hawkmoths were able to use characteristic odor-directed flight orientation and oviposit on the host plant. Overall, OR-mediated olfaction is essential for foraging and pollination behaviors, but plant-seeking and oviposition behaviors are sustained through additional OR-independent sensory cues.

Insects, including those which provide vital ecosystems services as well as those which are devastating pests or disease vectors, locate their resources mainly based on olfaction. Understanding insect olfaction not only from a neurobiological but also from an ecological perspective is therefore crucial to balance insect control and conservation. However, among all sensory stimuli olfaction is particularly hard to grasp. Our chemical environment is made up of thousands of different compounds, which might again be detected by our nose in multiple ways. Due to this complexity, researchers have only recently begun to explore the chemosensory ecology of model organisms such as Drosophila, linking the tools of chemical ecology to those of neurogenetics. This cross-disciplinary approach has enabled several studies that range from single odors and their ecological relevance, via olfactory receptor genes and neuronal processing, up to the insects' behavior. We learned that the insect olfactory system employs strategies of combinatorial coding to process general odors as well as labeled lines for specific compounds that call for an immediate response. These studies opened new doors to the olfactory world in which insects feed, oviposit, and mate.

Pollination by insects is essential to many ecosystems. Previously, we have shown that floral scent is important to mediate pollen transfer between plants (Kessler et al., 2015). Yet, the mechanisms by which pollinators evaluate volatiles of single flowers remained unclear. Here, Nicotiana attenuata plants, in which floral volatiles have been genetically silenced and its hawkmoth pollinator, Manduca sexta, were used in semi-natural tent and wind-tunnel assays to explore the function of floral scent. We found that floral scent functions to increase the fitness of individual flowers not only by increasing detectability but also by enhancing the pollinator's foraging efforts. Combining proboscis choice tests with neurophysiological, anatomical and molecular analyses we show that this effect is governed by newly discovered olfactory neurons on the tip of the moth's proboscis. With the tip of their tongue, pollinators assess the advertisement of individual flowers, an ability essential for maintaining this important ecosystem service.DOI: http://dx.doi.org/10.7554/eLife.15039.001

Cost efficient foraging is of especial importance for animals like hawkmoths or hummingbirds that are feeding ‘on the wing', making their foraging energetically demanding. The economic decisions made by these animals have a strong influence on the plants they pollinate and floral volatiles are often guiding these decisions. Here we show that the hawkmoth Manduca sexta exhibits an innate preference for volatiles of those Nicotiana flowers, which match the length of the moth's proboscis. This preference becomes apparent already at the initial inflight encounter, with the odour plume. Free-flight respiration analyses combined with nectar calorimetry revealed a significant caloric gain per invested flight energy only for preferred—matching—flowers. Our data therefore support Darwin's initial hypothesis on the coevolution of flower length and moth proboscis. We demonstrate that this interaction is mediated by an adaptive and hardwired olfactory preference of the moth for flowers offering the highest net-energy reward.