Large-scale characterization of sex pheromone communication systems in Drosophila.
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ABSTRACT:
SUBMITTER: Khallaf MA
PROVIDER: S-EPMC8260797 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:In many insect species, cuticular hydrocarbons serve as pheromones that can mediate complex social behaviors. In Drosophila melanogaster, several hydrocarbons including the male sex pheromone 11-cis-vaccenyl acetate (cVA) and female-specific 7,11-dienes influence courtship behavior and can function as cues for short-term memory associated with the mating experience. Behavioral and physiological studies suggest that other unidentified chemical communication cues are likely to exist. To more fully characterize the hydrocarbon profile of the D. melanogaster cuticle, we applied direct ultraviolet laser desorption/ionization orthogonal time-of-flight mass spectrometry (UV-LDI-o-TOF MS) and analyzed the surface of intact fruit flies at a spatial resolution of approximately 200 mum.We report the chemical and spatial characterization of 28 species of cuticular hydrocarbons, including a new major class of oxygen-containing compounds. Via UV-LDI MS, pheromones previously shown to be expressed exclusively by one sex, e.g., cVA, 7,11-heptacosadiene, and 7,11-nonacosadiene, appear to be found on both male and female flies. In males, cVA colocalizes at the tip of the ejaculatory bulb with a second acetylated hydrocarbon named CH503. We describe the chemical structure of CH503 as 3-O-acetyl-1,3-dihydroxy-octacosa-11,19-diene and demonstrate a behavioral role for this compound as a long-lived inhibitor of male courtship. Like cVA, CH503 is transferred from males to females during mating. Unlike cVA, CH503 remains on the surface of females for at least 10 days.Oxygenated hydrocarbons comprise a major previously undescribed class of compounds on the Drosophila cuticular surface. A newly discovered long-chain acetate, CH503, serves as a mediator of courtship-related chemical communication.
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Project description:It remains a conundrum in the evolution of sexual communication how the signals and responses can co-ordinate the changes during speciation. The genus Ostrinia contains several closely related species as well as distinctive strains with pheromone polymorphism and represents an example of ongoing speciation. Extensive studies in the genus, especially in the species the European corn borer O. nubilalis (ECB), the Asian corn borer O. furnacalis (ACB) and the adzuki bean borer O. scapulalis (ABB), have provided valuable insights into the evolution of sex pheromone communication. This review presents a comprehensive overview of the research on pheromone communication in different Ostrinia species over the past four decades, including pheromone identification and biosynthesis, the ligand profiles of pheromone receptor (PR) genes, the physiology of peripheral olfactory sensory neurons (OSNs) and the projection pattern to the antennal lobe. By integrating and comparing the closely related Ostrinia species and strains, it provides an evolutionary perspective on the sex pheromone communication in moths in general and also outlines the outstanding questions that await to be elucidated by future studies.
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Project description:The Drosophila pheromone cis-11-octadecenyl acetate (cVA) is used as pheromone throughout the melanogaster group and fulfils a primary role in sexual and social behaviours. Here, we found that Drosophila suzukii, an invasive pest that oviposits in undamaged ripe fruit, does not produce cVA. In fact, its production site, the ejaculatory bulb, is atrophied. Despite loss of cVA production, its receptor, Or67d, and cognate sensillum, T1, which are essential in cVA-mediated behaviours, were fully functional. However, T1 expression was dramatically reduced in D. suzukii, and the corresponding antennal lobe glomerulus, DA1, minute. Behavioural responses to cVA depend on the input balance of Or67d neurons (driving cVA-mediated behaviours) and Or65a neurons (inhibiting cVA-mediated behaviours). Accordingly, the shifted input balance in D. suzukii has reversed cVA's role in sexual behaviour: perfuming D. suzukii males with Drosophila melanogaster equivalents of cVA strongly reduced mating rates. cVA has thus evolved from a generic sex pheromone to a heterospecific signal that disrupts mating in D. suzukii, a saltational shift, mediated through offsetting the input balance that is highly conserved in congeneric species. This study underlines that dramatic changes in a species' sensory preference can result from rather 'simple' numerical shifts in underlying neural circuits.
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Project description:Long-range sex pheromones have been subjected to substantial research with a particular focus on their biosynthesis, peripheral perception, central processing and the resulting orientation behaviour of perceivers. Fundamental to the research on sex attractants was the assumption that they primarily coordinate species recognition. However, especially when they are produced by the less limiting sex (usually males), the evolution of heightened condition dependence might be expected and long-range sex pheromones might, therefore, also inform about a signaller's quality. Here we provide, to our knowledge, the first comprehensive study of the role of a male's long-range pheromone in mate choice that combines chemical analyses, video observations and field experiments with a multifactorial manipulation of males' condition. We show that the emission of the long-distance sex pheromone of the burying beetle, Nicrophorus vespilloides is highly condition-dependent and reliably reflects nutritional state, age, body size and parasite load--key components of an individual's somatic state. Both, the quantity and ratio of the pheromone components were affected but the time invested in pheromone emission was largely unaffected by a male's condition. Moreover, the variation in pheromone emission caused by the variation in condition had a strong effect on the attractiveness of males in the field, with males in better nutritional condition, of older age, larger body size and bearing less parasites being more attractive. That a single pheromone is influenced by so many aspects of the somatic state and causes such variation in a male's attractiveness under field conditions was hitherto unknown and highlights the need to integrate indicator models of sexual selection into pheromone research.
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Project description:The ecological effects of plant volatiles on herbivores are manifold. Little is known, however, about the impacts of non-host plant volatiles on intersexual pheromonal communication in specialist herbivores. We tested the effects of several prominent constitutive terpenoids released by conifers and Eucalyptus trees on electrophysiological and behavioral responses of an oligophagous species, Plutella xylostella, which feeds on Brassicaceae. The non-host plant volatile terpenoids adversely affected the calling behavior (pheromone emission) of adult females, and the orientation responses of adult males to sex pheromone were also significantly inhibited by these terpenoids in a wind tunnel and in the field. We suggest that disruption of both pheromone emission and orientation to sex pheromone may explain, at least in part, an observed reduction in herbivore attack in polyculture compared with monoculture plantings. We also propose that mating disruption of both male and female moths with non-host plant volatiles may be a promising alternative pest management strategy.
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Project description:Sex pheromone receptors (PRs) are key players in chemical communication between mating partners in insects. In the highly diversified insect order Lepidoptera, male PRs tuned to female-emitted type I pheromones (which make up the vast majority of pheromones identified) form a dedicated subfamily of odorant receptors (ORs). Here, using a combination of heterologous expression and in vivo genome editing methods, we bring functional evidence that at least one moth PR does not belong to this subfamily but to a distantly related OR lineage. This PR, identified in the cotton leafworm Spodoptera littoralis, is highly expressed in male antennae and is specifically tuned to the major sex pheromone component emitted by females. Together with a comprehensive phylogenetic analysis of moth ORs, our functional data suggest two independent apparitions of PRs tuned to type I pheromones in Lepidoptera, opening up a new path for studying the evolution of moth pheromone communication.
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Project description:A wide range of organisms use sex pheromones to communicate with each other and to identify appropriate mating partners. While the evolution of chemical communication has been suggested to cause sexual isolation and speciation, the mechanisms that govern evolutionary transitions in sex pheromone production are poorly understood. Here, we decipher the molecular mechanisms underlying the rapid evolution in the expression of a gene involved in sex pheromone production in Drosophilid flies. Long-chain cuticular hydrocarbons (e.g., dienes) are produced female-specifically, notably via the activity of the desaturase DESAT-F, and are potent pheromones for male courtship behavior in Drosophila melanogaster. We show that across the genus Drosophila, the expression of this enzyme is correlated with long-chain diene production and has undergone an extraordinary number of evolutionary transitions, including six independent gene inactivations, three losses of expression without gene loss, and two transitions in sex-specificity. Furthermore, we show that evolutionary transitions from monomorphism to dimorphism (and its reversion) in desatF expression involved the gain (and the inactivation) of a binding-site for the sex-determination transcription factor, DOUBLESEX. In addition, we documented a surprising example of the gain of particular cis-regulatory motifs of the desatF locus via a set of small deletions. Together, our results suggest that frequent changes in the expression of pheromone-producing enzymes underlie evolutionary transitions in chemical communication, and reflect changing regimes of sexual selection, which may have contributed to speciation among Drosophila.
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Project description: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.
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Project description:Dynamic interactions between remote but functionally specialized brain regions enable complex information processing. This intercortical communication is disrupted in the neural networks of patients with focal epilepsy, and epileptic activity can exert widespread effects within the brain. Using large-scale human intracranial electroencephalography recordings, we show that interictal epileptiform discharges (IEDs) are significantly coupled with spindles in discrete, individualized brain regions outside of the epileptic network. We found that a substantial proportion of these localized spindles travel across the cortical surface. Brain regions that participate in this IED-driven oscillatory coupling express spindles that have a broader spatial extent and higher tendency to propagate than spindles occurring in uncoupled regions. These altered spatiotemporal oscillatory properties identify areas that are shaped by epileptic activity independent of IED or seizure detection. Our findings suggest that IED-spindle coupling may be an important mechanism of interictal global network dysfunction that could be targeted to prevent disruption of normal neural activity.
| S-EPMC6821283 | biostudies-literature
Project description:The detection and processing of chemical stimuli involve coordinated neuronal networks that process sensory information. This allows animals, such as the model species Drosophila melanogaster, to detect food sources and to choose a potential mate. In peripheral olfactory tissues, several classes of proteins are acting to modulate the detection of chemosensory signals. This includes odorant-binding proteins together with odorant-degrading enzymes (ODEs). These enzymes, which primarily act to eliminate toxic compounds from the whole organism also modulate chemodetection. ODEs are thought to neutralize the stimulus molecule concurrently to its detection, avoiding receptor saturation thus allowing chemosensory neurons to respond to the next stimulus. Here, we show that one UDP-glycosyltransferase (UGT36E1) expressed in D. melanogaster antennal olfactory sensory neurons (OSNs) is involved in sex pheromone discrimination. UGT36E1 overexpression caused by an insertion mutation affected male behavioral ability to discriminate sex pheromones while it increased OSN electrophysiological activity to male pheromones. Reciprocally, the decreased expression of UGT36E1, controlled by an RNAi transgene, improved male ability to discriminate sex pheromones whereas it decreased electrophysiological activity in the relevant OSNs. When we combined the two genotypes (mutation and RNAi), we restored wild-type-like levels both for the behavioral discrimination and UGT36E1 expression. Taken together, our results strongly suggest that this UGT plays a pivotal role in Drosophila pheromonal detection.
| S-EPMC7140800 | biostudies-literature