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The codling moth, Cydia pomonella, is an important fruit pest worldwide. As nocturnal animals, adults depend to a large extent on olfactory cues for detection of food and mates, and, for females, oviposition sites. In insects, odor detection is mediated by odorant receptors (ORs) and ionotropic receptors (IRs), which ensure the specificity of the olfactory sensory neuron responses. In this study, our aim was to identify chemosensory receptors in the codling moth as a means to uncover new targets for behavioral interference. Using next-generation sequencing techniques, we identified a total of 43 candidate ORs, one gustatory receptor and 15 IRs in the antennal transcriptome. Through Blast and sequence similarity analyses we annotated the insect obligatory co-receptor ORco, five genes clustering in a conserved clade containing sex pheromone receptors, one homolog of the Bombyx mori female-enriched receptor BmorOR30 (but no homologs of the other B. mori female-enriched receptors) and one gene clustering in the sugar receptor family. Among the candidate IRs, we identified homologs of the two highly conserved co-receptors IR8a and IR25a, and one homolog of an IR involved in phenylethyl amine detection in Drosophila. Our results open for functional characterization of the chemosensory receptors of C. pomonella, with potential for new or refined applications of semiochemicals for control of this pest insect.

1. The highly invasive spotted wing Drosophila Drosophila suzukii is a key pest of soft fruit and berries in Europe and North America, and development of control techniques is an urgent research challenge. Drosophila suzukii is widely associated with the yeast Hanseniaspora uvarum. Yeasts are symbionts of drosophilid flies and communicate with insects through volatile metabolites for spore dispersal. Accordingly, yeasts and behaviour-modifying chemicals produced by yeasts are prospective tools for environmentally sound insect management. 2. We first bioassayed flight attraction, feeding and oviposition of D. suzukii females in response to H. uvarum yeast and blueberries, which are a preferred host fruit. We then investigated the combined effect of yeast and insecticide on adult female oviposition behaviour and mortality towards the development of a yeast-based control method. 3. Following mating, attraction of female flies to blueberry and yeast odour cues was strongly enhanced. Yeast feeding significantly increased in mated females, while yeast did not increase oviposition on blueberries. This observation suggests that mated flies become attracted to yeast for feeding and to fruit for egg laying. A combined feeding-oviposition assay demonstrated different roles and interference between yeast and fruit stimuli: during the day after mating, females laid fewer eggs when yeast was available. 4. The post-mating yeast-feeding response is an opportunity for the development of an attract-and-kill technique for population control of D. suzukii. Exposing flies to a blend of yeast and insecticide reduced oviposition and greatly enhanced adult fly mortality compared with an insecticide treatment alone. 5. Synthesis and applications. Mated females are the key life stage for Drosophila suzukii population control. Egg-laying females perforate fruit skin and fungal infestations ensue, even when eggs and larvae are killed off by insecticide sprays. Behaviour-modifying chemicals, including yeast metabolites, enable environmentally safe insect management via manipulation of olfactory-mediated reproductive behaviour. Our results highlight that yeast and yeast semiochemicals hold potential for D. suzukii management and that response modulation to olfactory stimuli following mating is a vital element for the development of D. suzukii control methods. Yeast feeding is enhanced in mated D. suzukii females, and this change in post-mating behaviour can be exploited by an attract-and-kill strategy, combining a fly-associated yeast with an insecticide. Furthermore, using the D. suzukii yeast mutualist, H. uvarum, may reduce non-target effects and increase species specificity, which further contributes to the development of an efficient and safe control method.

1. Plants produce herbivore-induced plant volatiles (HIPVs) in response to damage by herbivores. Although HIPVs are known to enhance plant resistance by affecting herbivore host plant preferences and by attracting natural enemies, little is known about the role of HIPVs on the resistance of neighbouring plants and the mechanism behind this associational resistance. 2. This study examined the effect of HIPVs from herbivore-damaged host plants (alfalfa (Medicago sativa), clover (Trifolium alexandrinum) and cotton (Gossypium hirsutum)) on oviposition by Egyptian cotton leafworm (Spodoptera littoralis) (Lepidoptera: Noctuidae) on neighbouring, undamaged host plants. 3. There was a significant reduction in oviposition by S. littoralis on undamaged plants adjacent to herbivore-damaged cotton plants under both field and laboratory conditions. The results showed that the associational resistance by HIPVs depends on direct effects on oviposition behaviour in S. littoralis.There were also indications that other mechanisms may be involved. 4. Associational resistance via HIPVs was not observed for all plant species tested. Emission of HIPVs from damaged cotton increased the resistance of undamaged cotton and alfalfa plants to oviposition by S. littoralis, but HIPVs from damaged alfalfa and clover neighbours did not provide resistance to undamaged cotton plants. 5. Synthesis. Our results suggest that the presence of HIPV-emitting plant neighbours can reduce herbivory on undamaged plants and enhance plant resistance by affecting oviposition behaviour in insect herbivores.

Mating induces profound physiological changes in a wide range of insects, leading to behavioural adjustments to match the internal state of the animal. Here, we show for the first time, to our knowledge, that a noctuid moth switches its olfactory response from food to egg-laying cues following mating. Unmated females of the cotton leafworm (Spodoptera littoralis) are strongly attracted to lilac flowers (Syringa vulgaris). After mating, attraction to floral odour is abolished and the females fly instead to green-leaf odour of the larval host plant cotton, Gossypium hirsutum. This behavioural switch is owing to a marked change in the olfactory representation of floral and green odours in the primary olfactory centre, the antennal lobe (AL). Calcium imaging, using authentic and synthetic odours, shows that the ensemble of AL glomeruli dedicated to either lilac or cotton odour is selectively up- and downregulated in response to mating. A clear-cut behavioural modulation as a function of mating is a useful substrate for studies of the neural mechanisms underlying behavioural decisions. Modulation of odour-driven behaviour through concerted regulation of odour maps contributes to our understanding of state-dependent choice and host shifts in insect herbivores.

Background Mate finding and recognition in animals evolves during niche adaptation and involves social signals and habitat cues. Drosophila melanogaster and related species are known to be attracted to fermenting fruit for feeding and egg-laying, which poses the question of whether species-specific fly odours contribute to long-range premating communication. Results We have discovered an olfactory channel in D. melanogaster with a dual affinity to sex and food odorants. Female flies release a pheromone, ( Z )-4-undecenal ( Z 4-11Al), that elicits flight attraction in both sexes. Its biosynthetic precursor is the cuticular hydrocarbon ( Z,Z )-7,11-heptacosadiene (7,11-HD), which is known to afford reproductive isolation between the sibling species D. melanogaster and D. simulans during courtship. Twin olfactory receptors, Or69aB and Or69aA, are tuned to Z 4-11Al and food odorants, respectively. They are co-expressed in the same olfactory sensory neurons, and feed into a neural circuit mediating species-specific, long-range communication; however, the close relative D. simulans , which shares food resources with D. melanogaster , does not respond to Z 4-11Al. Conclusion The Or69aA and Or69aB isoforms have adopted dual olfactory traits. The underlying gene yields a collaboration between natural and sexual selection, which has the potential to drive speciation.

The fruit fly, Drosophila melanogaster Meigen (Diptera: Drosophilidae), is a model for how animals sense, discriminate, and respond to chemical signals. However, with D. melanogaster our knowledge of the behavioral activity of olfactory receptor ligands has relied largely on close-range attraction, rather than on long-range orientation behavior. We developed a flight assay to relate chemosensory perception to behavior. Headspace volatiles from vinegar attracted 62% of assayed flies during a 15-min experimental period. Flies responded irrespective of age, sex, and mating state, provided they had been starved. To identify behaviorally relevant chemicals from vinegar, we compared the responses to vinegar and synthetic chemicals. Stimuli were applied by a piezoelectric sprayer at known and constant release rates. Re-vaporized methanol extracts of Super Q-trapped vinegar volatiles attracted as many flies as vinegar. The main volatile component of vinegar, acetic acid, elicited significant attraction as a single compound. Two other vinegar volatiles, 2-phenyl ethanol and acetoin, produced a synergistic effect when added to acetic acid. Geosmin, a microbiological off-flavor, diminished attraction to vinegar. This wind tunnel assay based on a conspicuous and unambiguous behavioral response provides the necessary resolution for the investigation of physiologically and ecologically relevant odors and will become an essential tool for the functional analysis of the D. melanogaster olfactory system.

In Drosophila melanogaster , gender-specific behavioural responses to the male-produced sex pheromone cis -vaccenyl acetate (cVA) rely on sexually dimorphic, third-order neural circuits. We show that nutritional state in female flies modulates cVA perception in first-order olfactory neurons. Starvation increases and feeding reduces attraction to food odour, in both sexes. Adding cVA to food odour, however, maintains attraction in fed females, while it has no effect in males. Upregulation of sensitivity and behavioural responsiveness to cVA in fed females is paralleled by a strong increase in receptivity to male courtship. Functional imaging of the antennal lobe (AL), the olfactory centre in the insect brain, shows that olfactory input to DA1 and VM2 glomeruli is also modulated by starvation. Knocking down insulin receptors in neurons converging onto the DA1 glomerulus suggests that insulin-signalling partly controls pheromone perception in the AL and adjusts cVA attraction according to nutritional state and sexual receptivity in Drosophila females.

A high reproductive potential is one reason for the rapid spread of Drosophila suzukii in Europe and in the United States. In order to identify mechanisms that mediate mating and reproduction in D. suzukii we studied the fly’s reproductive behavior, diurnal mating activity and sexual maturation. Furthermore, we studied the change of female cuticular hydrocarbons (CHCs) with age and conducted a preliminary investigation on the role of female-derived chemical signals in male mating behavior. Sexual behavior in D. suzukii is characterized by distinct elements of male courtship leading to female acceptance for mating. Time of day and age modulate D. suzukii mating activity. As with other drosophilids, female sexual maturity is paralleled by a quantitative increase in CHCs. Neither female CHCs nor other olfactory signals were required to induce male courtship, however, presence of those signals significantly increased male sexual behavior. With this pilot study we hope to stimulate research on the reproductive biology of D. suzukii, which is relevant for the development of pest management tools.

The idea of using species-specific behavior-modifying chemicals for the management of noxious insects in agriculture, horticulture, forestry, stored products, and for insect vectors of diseases has been a driving ambition through five decades of pheromone research. Hundreds of pheromones and other semiochemicals have been discovered that are used to monitor the presence and abundance of insects and to protect plants and animals against insects. The estimated annual production of lures for monitoring and mass trapping is on the order of tens of millions, covering at least 10 million hectares. Insect populations are controlled by air permeation and attract-and-kill techniques on at least 1 million hectares. Here, we review the most important and widespread practical applications. Pheromones are increasingly efficient at low population densities, they do not adversely affect natural enemies, and they can, therefore, bring about a long-term reduction in insect populations that cannot be accomplished with conventional insecticides. A changing climate with higher growing season temperatures and altered rainfall patterns makes control of native and invasive insects an increasingly urgent challenge. Intensified insecticide use will not provide a solution, but pheromones and other semiochemicals instead can be implemented for sustainable area-wide management and will thus improve food security for a growing population. Given the scale of the challenges we face to mitigate the impacts of climate change, the time is right to intensify goal-oriented interdisciplinary research on semiochemicals, involving chemists, entomologists, and plant protection experts, in order to provide the urgently needed, and cost-effective technical solutions for sustainable insect management worldwide.

The search for mates and food is mediated by volatile chemicals. Insects sense food odorants and sex pheromones through odorant receptors (ORs) and pheromone receptors (PRs), which are expressed in olfactory sensory neurons. Molecular phylogenetics of ORs, informed by behavioral and functional data, generates sound hypotheses for the identification of semiochemicals driving olfactory behavior. Studying orthologous receptors and their ligands across taxa affords insights into the role of chemical communication in reproductive isolation and phylogenetic divergence. The female sex pheromone of green budworm moth Hedya nubiferana (Lepidoptera, Totricidae) is a blend of two unsaturated acetates, only a blend of both elicits male attraction. Females produce in addition codlemone, which is the sex pheromone of another tortricid, codling moth Cydia pomonella. Codlemone also attracts green budworm moth males. Concomitantly, green budworm and codling moth males are attracted to the host plant volatile pear ester. A congruent behavioral response to the same pheromone and plant volatile in two tortricid species suggests co‐occurrence of dedicated olfactory channels. In codling moth, one PR is tuned to both compounds, the sex pheromone codlemone and the plant volatile pear ester. Our phylogenetic analysis finds that green budworm moth expresses an orthologous PR gene. Shared ancestry, and high levels of amino acid identity and sequence similarity, in codling and green budworm moth PRs offer an explanation for parallel attraction of both species to the same compounds. A conserved olfactory channel for a sex pheromone and a host plant volatile substantiates the alliance of social and habitat signals in insect chemical communication. Field attraction assays confirm that in silico investigations of ORs afford powerful predictions for an efficient identification of behavior‐modifying semiochemicals, for an improved understanding of the mechanisms of host plant attraction in insect herbivores and for the further development of sustainable insect control. Hedya nubiferana (a tortricid moth on apple and other rosacean plants) is attracted to the sex pheromone and to the plant‐derived kairomone of codling moth (another tortricid moth feeding on apple). A conserved odorant receptor is the basis for this coincidence, which demonstrates the interaction of social signals and food cues in insect herbivores.