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An Inhibitory Sex Pheromone Tastes Bitter for Drosophila Males  [PDF]
Fabien Lacaille, Makoto Hiroi, Robert Twele, Tsuyoshi Inoshita, Daisuke Umemoto, Gérard Manière, Frédéric Marion-Poll, Mamiko Ozaki, Wittko Francke, Matthew Cobb, Claude Everaerts, Teiichi Tanimura, Jean-Fran?ois Ferveur
PLOS ONE , 2007, DOI: 10.1371/journal.pone.0000661
Abstract: Sexual behavior requires animals to distinguish between the sexes and to respond appropriately to each of them. In Drosophila melanogaster, as in many insects, cuticular hydrocarbons are thought to be involved in sex recognition and in mating behavior, but there is no direct neuronal evidence of their pheromonal effect. Using behavioral and electrophysiological measures of responses to natural and synthetic compounds, we show that Z-7-tricosene, a Drosophila male cuticular hydrocarbon, acts as a sex pheromone and inhibits male-male courtship. These data provide the first direct demonstration that an insect cuticular hydrocarbon is detected as a sex pheromone. Intriguingly, we show that a particular type of gustatory neurons of the labial palps respond both to Z-7-tricosene and to bitter stimuli. Cross-adaptation between Z-7-tricosene and bitter stimuli further indicates that these two very different substances are processed by the same neural pathways. Furthermore, the two substances induced similar behavioral responses both in courtship and feeding tests. We conclude that the inhibitory pheromone tastes bitter to the fly.
Natural Variation in the Strength and Direction of Male Mating Preferences for Female Pheromones in Drosophila melanogaster  [PDF]
Alison Pischedda, Michael P. Shahandeh, Wesley G. Cochrane, Veronica A. Cochrane, Thomas L. Turner
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0087509
Abstract: Many animal species communicate using chemical signals. In Drosophila, cuticular hydrocarbons (CHCs) are involved in species and sexual identification, and have long been thought to act as stimulatory pheromones as well. However, a previous study reported that D. melanogaster males were more attracted to females that were lacking CHCs. This surprising result is consistent with several evolutionary hypotheses but is at odds with other work demonstrating that female CHCs are attractive to males. Here, we investigated natural variation in male preferences for female pheromones using transgenic flies that cannot produce CHCs. By perfuming females with CHCs and performing mate choice tests, we found that some male genotypes prefer females with pheromones, some have no apparent preference, and at least one male genotype prefers females without pheromones. This variation provides an excellent opportunity to further investigate the mechanistic causes and evolutionary implications of divergent pheromone preferences in D. melanogaster males.
Rapid Evolution of Sex Pheromone-Producing Enzyme Expression in Drosophila  [PDF]
Troy R. Shirangi,Hélo?se D. Dufour,Thomas M. Williams,Sean B. Carroll
PLOS Biology , 2012, DOI: 10.1371/journal.pbio.1000168
Abstract: 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.
Rapid Evolution of Sex Pheromone-Producing Enzyme Expression in Drosophila  [PDF]
Troy R. Shirangi equal contributor,Hélo?se D. Dufour equal contributor,Thomas M. Williams,Sean B. Carroll
PLOS Biology , 2009, DOI: 10.1371/journal.pbio.1000168
Abstract: 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.
Volatile Drosophila Cuticular Pheromones Are Affected by Social but Not Sexual Experience  [PDF]
Jean-Pierre Farine, Jean-Fran?ois Ferveur, Claude Everaerts
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0040396
Abstract: Recognition of conspecifics and mates is based on a variety of sensory cues that are specific to the species, sex and social status of each individual. The courtship and mating activity of Drosophila melanogaster flies is thought to depend on the olfactory perception of a male-specific volatile pheromone, cis-vaccenyl acetate (cVA), and the gustatory perception of cuticular hydrocarbons (CHs), some of which are sexually dimorphic. Using two complementary sampling methods (headspace Solid Phase Micro-Extraction [SPME] and solvent extraction) coupled with GC-MS analysis, we measured the dispersion of pheromonal CHs in the air and on the substrate around the fly. We also followed the variations in CHs that were induced by social and sexual interactions. We found that all CHs present on the fly body were deposited as a thin layer on the substrate, whereas only a few of these molecules were also detected in the air. Moreover, social experience during early adult development and in mature flies strongly affected male volatile CHs but not cVA, whereas sexual interaction only had a moderate influence on dispersed CHs. Our study suggests that, in addition to their role as contact cues, CHs can influence fly behavior at a distance and that volatile, deposited and body pheromonal CHs participate in a three-step recognition of the chemical identity and social status of insects.
Cuticular Hydrocarbon Content that Affects Male Mate Preference of Drosophila melanogaster from West Africa  [PDF]
Aya Takahashi,Nao Fujiwara-Tsujii,Ryohei Yamaoka,Masanobu Itoh,Mamiko Ozaki,Toshiyuki Takano-Shimizu
International Journal of Evolutionary Biology , 2012, DOI: 10.1155/2012/278903
Abstract: Intraspecific variation in mating signals and preferences can be a potential source of incipient speciation. Variable crossability between Drosophila melanogaster and D. simulans among different strains suggested the abundance of such variations. A particular focus on one combination of D. melanogaster strains, TW1(G23) and Mel6(G59), that showed different crossabilities to D. simulans, revealed that the mating between females from the former and males from the latter occurs at low frequency. The cuticular hydrocarbon transfer experiment indicated that cuticular hydrocarbons of TW1 females have an inhibitory effect on courtship by Mel6 males. A candidate component, a C25 diene, was inferred from the gas chromatography analyses. The intensity of male refusal of TW1 females was variable among different strains of D. melanogaster, which suggested the presence of variation in sensitivity to different chemicals on the cuticle. Such variation could be a potential factor for the establishment of premating isolation under some conditions. 1. Introduction Drosophila exhibits complex mating behavior with frequent wing vibration and copulation attempts by males. The successful mating is achieved by communications between males and females using chemical, acoustic, and visual signals (reviewed in [1]). Subtle differences in these signals may accumulate during or after the formation of reproductive isolation. Once reproduction isolation is established to a certain extent, the correct mate recognition is essential to avoid costly hybridization and wasting time on unsuccessful courtship. Indeed, a certain degree of premating isolation or mating incompatibility is commonly observed between closely related species of Drosophila [2, 3]. In some cosmopolitan species of Drosophila, for example, D. ananassae [4] and D. elegans [5, 6], widely observed mating incompatibilities between populations from different locations exist. The degree of incompatibility is variable among sampled strains in these species. Another cosmopolitan species, D. melanogaster, also harbors incompatible combinations of populations [7–11]. The degree of incompatibility between populations is also variable, and many intermediate strains are typically observed. These within species incompatibilities suggest that there are many intraspecific variations in mating signals and preferences. Those variations could either fix in isolated populations or become targets of sexual selection under some conditions and consequently result in divergent mating-associated characters among different populations. It is
A Model-Based Analysis of Chemical and Temporal Patterns of Cuticular Hydrocarbons in Male Drosophila melanogaster  [PDF]
Clement Kent, Reza Azanchi, Ben Smith, Adrienne Chu, Joel Levine
PLOS ONE , 2007, DOI: 10.1371/journal.pone.0000962
Abstract: Drosophila Cuticular Hydrocarbons (CH) influence courtship behaviour, mating, aggregation, oviposition, and resistance to desiccation. We measured levels of 24 different CH compounds of individual male D. melanogaster hourly under a variety of environmental (LD/DD) conditions. Using a model-based analysis of CH variation, we developed an improved normalization method for CH data, and show that CH compounds have reproducible cyclic within-day temporal patterns of expression which differ between LD and DD conditions. Multivariate clustering of expression patterns identified 5 clusters of co-expressed compounds with common chemical characteristics. Turnover rate estimates suggest CH production may be a significant metabolic cost. Male cuticular hydrocarbon expression is a dynamic trait influenced by light and time of day; since abundant hydrocarbons affect male sexual behavior, males may present different pheromonal profiles at different times and under different conditions.
Genes Involved in Sex Pheromone Discrimination in Drosophila melanogaster and Their Background-Dependent Effect  [PDF]
Benjamin Houot, Stéphane Fraichard, Ralph J. Greenspan, Jean-Fran?ois Ferveur
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0030799
Abstract: Mate choice is based on the comparison of the sensory quality of potential mating partners, and sex pheromones play an important role in this process. In Drosophila melanogaster, contact pheromones differ between male and female in their content and in their effects on male courtship, both inhibitory and stimulatory. To investigate the genetic basis of sex pheromone discrimination, we experimentally selected males showing either a higher or lower ability to discriminate sex pheromones over 20 generations. This experimental selection was carried out in parallel on two different genetic backgrounds: wild-type and desat1 mutant, in which parental males showed high and low sex pheromone discrimination ability respectively. Male perception of male and female pheromones was separately affected during the process of selection. A comparison of transcriptomic activity between high and low discrimination lines revealed genes not only that varied according to the starting genetic background, but varied reciprocally. Mutants in two of these genes, Shaker and quick-to-court, were capable of producing similar effects on discrimination on their own, in some instances mimicking the selected lines, in others not. This suggests that discrimination of sex pheromones depends on genes whose activity is sensitive to genetic context and provides a rare, genetically defined example of the phenomenon known as “allele flips,” in which interactions have reciprocal effects on different genetic backgrounds.
cuticleDB: a relational database of Arthropod cuticular proteins
Christiana K Magkrioti, Ioannis C Spyropoulos, Vassiliki A Iconomidou, Judith H Willis, Stavros J Hamodrakas
BMC Bioinformatics , 2004, DOI: 10.1186/1471-2105-5-138
Abstract: Most of these cuticular protein sequences contain motifs found only in arthropod proteins.cuticleDB is a relational database containing all structural proteins of Arthropod cuticle identified to date. Many come from direct sequencing of proteins isolated from cuticle and from sequences from cDNAs that share common features with these authentic cuticular proteins. It also includes proteins from the Drosophila melanogaster and the Anopheles gambiae genomes, that have been predicted to be cuticular proteins, based on a Pfam motif (PF00379) responsible for chitin binding in Arthropod cuticle. The total number of the database entries is 445: 370 derive from insects, 60 from Crustacea and 15 from Chelicerata. The database can be accessed from our web server at http://bioinformatics.biol.uoa.gr/cuticleDB webcite.CuticleDB was primarily designed to contain correct and full annotation of cuticular protein data. The database will be of help to future genome annotators. Users will be able to test hypotheses for the existence of known and also of yet unknown motifs in cuticular proteins. An analysis of motifs may contribute to understanding how proteins contribute to the physical properties of cuticle as well as to the precise nature of their interaction with chitin.One particular family of cuticular proteins constitutes one of the largest multigene families known in insects [1]. Unrelated cuticular proteins are also numerous within a single species [2,3]. This diversity of cuticular proteins is extraordinary when one considers that chitin, the other principal constituent of cuticle, is a simple filamentous polymer of N-acetylglucosamine. Over 60 sequences have been obtained from proteins extracted from arthropod cuticles freed from adhering cells, primarily through the work of Svend Andersen and his colleagues in Copenhagen. An additional 9 have been extracted from cuticle and had their N-terminal sequences determined [2,3]. These verified cuticular protein sequences revealed
Drosophila Cuticular Hydrocarbons Revisited: Mating Status Alters Cuticular Profiles  [PDF]
Claude Everaerts,Jean-Pierre Farine,Matthew Cobb,Jean-Fran?ois Ferveur
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0009607
Abstract: Most living organisms use pheromones for inter-individual communication. In Drosophila melanogaster flies, several pheromones perceived either by contact/at a short distance (cuticular hydrocarbons, CHs), or at a longer distance (cis-vaccenyl acetate, cVA), affect courtship and mating behaviours. However, it has not previously been possible to precisely identify all potential pheromonal compounds and simultaneously monitor their variation on a time scale. To overcome this limitation, we combined Solid Phase Micro-Extraction with gas-chromatography coupled with mass-spectrometry. This allowed us (i) to identify 59 cuticular compounds, including 17 new CHs; (ii) to precisely quantify the amount of each compound that could be detected by another fly, and (iii) to measure the variation of these substances as a function of aging and mating. Sex-specific variation appeared with age, while mating affected cuticular compounds in both sexes with three possible patterns: variation was (i) reciprocal in the two sexes, suggesting a passive mechanical transfer during mating, (ii) parallel in both sexes, such as for cVA which strikingly appeared during mating, or (iii) unilateral, presumably as a result of sexual interaction. We provide a complete reassessment of all Drosophila CHs and suggest that the chemical conversation between male and female flies is far more complex than is generally accepted. We conclude that focusing on individual compounds will not provide a satisfactory understanding of the evolution and function of chemical communication in Drosophila.
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