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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
Genotype-by-Environment Interactions for Female Mate Choice of Male Cuticular Hydrocarbons in Drosophila simulans  [PDF]
Fiona C. Ingleby, John Hunt, David J. Hosken
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0067623
Abstract: Recent research has highlighted the potential importance of environmental and genotype-by-environment (G×E) variation in sexual selection, but most studies have focussed on the expression of male sexual traits. Consequently, our understanding of genetic variation for plasticity in female mate choice is extremely poor. In this study we examine the genetics of female mate choice in Drosophila simulans using isolines reared across two post-eclosion temperatures. There was evidence for G×Es in female choosiness and preference, which suggests that the evolution of female mate choice behaviour could differ across environments. However, the ranked order of preferred males was consistent across females and environments, so the same males are favoured by mate choice in spite of G×Es. Our study highlights the importance of taking cross-environment perspectives in order to gain a more comprehensive understanding of the operation of sexual selection.
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.
Male-Specific Transfer and Fine Scale Spatial Differences of Newly Identified Cuticular Hydrocarbons and Triacylglycerides in a Drosophila Species Pair  [PDF]
Joanne Y. Yew,Klaus Dreisewerd,Cássia Cardoso de Oliveira,William J. Etges
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0016898
Abstract: We analyzed epicuticular hydrocarbon variation in geographically isolated populations of D. mojavensis cultured on different rearing substrates and a sibling species, D. arizonae, with ultraviolet laser desorption/ionization mass spectrometry (UV-LDI MS). Different body parts, i.e. legs, proboscis, and abdomens, of both species showed qualitatively similar hydrocarbon profiles consisting mainly of long-chain monoenes, dienes, trienes, and tetraenes. However, D. arizonae had higher amounts of most hydrocarbons than D. mojavensis and females of both species exhibited greater hydrocarbon amounts than males. Hydrocarbon profiles of D. mojavensis populations were significantly influenced by sex and rearing substrates, and differed between body parts. Lab food–reared flies had lower amounts of most hydrocarbons than flies reared on fermenting cactus substrates. We discovered 48 male- and species-specific hydrocarbons ranging in size from C22 to C50 in the male anogenital region of both species, most not described before. These included several oxygen-containing hydrocarbons in addition to high intensity signals corresponding to putative triacylglycerides, amounts of which were influenced by larval rearing substrates. Some of these compounds were transferred to female cuticles in high amounts during copulation. This is the first study showing that triacylglycerides may be a separate class of courtship-related signaling molecules in drosophilids. This study also extends the kind and number of epicuticular hydrocarbons in these species and emphasizes the role of larval ecology in influencing amounts of these compounds, many of which mediate courtship success within and between species.
Dietary Effects on Cuticular Hydrocarbons and Sexual Attractiveness in Drosophila  [PDF]
Tatyana Y. Fedina, Tsung-Han Kuo, Klaus Dreisewerd, Herman A. Dierick, Joanne Y. Yew, Scott D. Pletcher
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0049799
Abstract: Dietary composition is known to have profound effects on many aspects of animal physiology, including lifespan, general health, and reproductive potential. We have previously shown that aging and insulin signaling significantly influence the composition and sexual attractiveness of Drosophila melanogaster female cuticular hydrocarbons (CHCs), some of which are known to be sex pheromones. Because diet is intimately linked to aging and to the activity of nutrient-sensing pathways, we asked how diet affects female CHCs and attractiveness. Here we report consistent and significant effects of diet composition on female CHC profiles across ages, with dietary yeast and sugar driving CHC changes in opposite directions. Surprisingly, however, we found no evidence that these changes affect female attractiveness. Multivariate comparisons among responses of CHC profiles to diet, aging, and insulin signaling suggest that diet may alter the levels of some CHCs in a way that results in profiles that are more attractive while simultaneously altering other CHCs in a way that makes them less attractive. For example, changes in short-chain CHCs induced by a high-yeast diet phenocopy changes caused by aging and by decreased insulin signaling, both of which result in less attractive females. On the other hand, changes in long-chain CHCs in response to the same diet result in levels that are comparable to those observed in attractive young females and females with increased insulin signaling. The effects of a high-sugar diet tend in the opposite direction, as levels of short-chain CHCs resemble those in attractive females with increased insulin signaling and changes in long-chain CHCs are similar to those caused by decreased insulin signaling. Together, these data suggest that diet-dependent changes in female CHCs may be sending conflicting messages to males.
Peripheral, Central and Behavioral Responses to the Cuticular Pheromone Bouquet in Drosophila melanogaster Males  [PDF]
Tsuyoshi Inoshita,Jean-René Martin,Frédéric Marion-Poll,Jean-Fran?ois Ferveur
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0019770
Abstract: Pheromonal communication is crucial with regard to mate choice in many animals including insects. Drosophila melanogaster flies produce a pheromonal bouquet with many cuticular hydrocarbons some of which diverge between the sexes and differently affect male courtship behavior. Cuticular pheromones have a relatively high weight and are thought to be — mostly but not only — detected by gustatory contact. However, the response of the peripheral and central gustatory systems to these substances remains poorly explored. We measured the effect induced by pheromonal cuticular mixtures on (i) the electrophysiological response of peripheral gustatory receptor neurons, (ii) the calcium variation in brain centers receiving these gustatory inputs and (iii) the behavioral reaction induced in control males and in mutant desat1 males, which show abnormal pheromone production and perception. While male and female pheromones induced inhibitory-like effects on taste receptor neurons, the contact of male pheromones on male fore-tarsi elicits a long-lasting response of higher intensity in the dedicated gustatory brain center. We found that the behavior of control males was more strongly inhibited by male pheromones than by female pheromones, but this difference disappeared in anosmic males. Mutant desat1 males showed an increased sensitivity of their peripheral gustatory neurons to contact pheromones and a behavioral incapacity to discriminate sex pheromones. Together our data indicate that cuticular hydrocarbons induce long-lasting inhibitory effects on the relevant taste pathway which may interact with the olfactory pathway to modulate pheromonal perception.
Variation in the Male Pheromones and Mating Success of Wild Caught Drosophila melanogaster  [PDF]
David Scott, Alicia Shields, Michaela Straker, Heidi Dalrymple, Priya K. Dhillon, Singh Harbinder
PLOS ONE , 2011, DOI: 10.1371/journal.pone.0023645
Abstract: Drosophila melanogaster males express two primary cuticular hydrocarbons (male-predominant hydrocarbons). These act as sex pheromones by influencing female receptivity to mating. The relative quantities of these hydrocarbons vary widely among natural populations and can contribute to variation in mating success. We tested four isofemale lines collected from a wild population to assess the effect of intrapopulation variation in male-predominant hydrocarbons on mating success. The receptivity of laboratory females to males of the four wild-caught lines varied significantly, but not consistently in the direction predicted by variation in male-predominant hydrocarbons. Receptivity of the wild-caught females to laboratory males also varied significantly, but females from lines with male-predominant hydrocarbon profiles closer to a more cosmopolitan one did not show a correspondingly strong mating bias toward a cosmopolitan male. Among wild-caught lines, the male-specific ejaculatory bulb lipid, cis-vaccenyl acetate, varied more than two-fold, but was not associated with variation in male mating success. We observed a strong inverse relationship between the receptivity of wild-caught females and the mating success of males from their own lines, when tested with laboratory flies of the opposite sex.
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.
Variation in Male Mate Choice in Drosophila melanogaster  [PDF]
Dominic A. Edward, Tracey Chapman
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0056299
Abstract: Male mate choice has been reported in the fruit fly, Drosophila melanogaster, even though males of this species were previously thought to maximise their fitness by mating with all available females. To understand the evolution of male mate choice it is important to understand variation in male mating preferences. Two studies, using different stock populations and different methods, have reported contrasting patterns of variation in male mate choice in D. melanogaster. Two possible explanations are that there are evolved differences in each stock population or that the methods used to measure choice could have biased the results. We investigated these hypotheses here by repeating the methods used in one study in which variable male mate choice was found, using the stock population from the other study in which choice was not variable. The results showed a significant resource-independent male preference for less fecund, smaller females, which contrasts with previous observations of male mate choice. This indicates that different selection pressures between populations have resulted in evolved differences in the expression of male mate choice. It also reveals phenotypic plasticity in male mate choice in response to cues encountered in each choice environment. The results highlight the importance of variation in male mate choice, and of identifying mechanisms in order to understand the evolution of mate choice under varying ecological conditions.
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.
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