Chemical cues that guide female reproduction in <i>Drosophila melanogaster</i>

Chemicals released into the environment by food, predators and conspecifics play critical roles in Drosophila reproduction. Females and males live in an environment full of smells, whose molecules communicate to them the availability of food, potential mates, competitors or predators. Volatile chemicals derived from fruit, yeast growing on the fruit, and flies already present on the fruit attract Drosophila, concentrating flies at food sites, where they will also mate. Species-specific cuticular hydrocarbons displayed on female Drosophila as they mature are sensed by males and act as pheromones to stimulate mating by conspecific males and inhibit heterospecific mating. The pheromonal profile of a female is also responsive to her nutritional environment, providing an honest signal of her fertility potential. After mating, cuticular and semen hydrocarbons transferred by the male change the female's chemical profile. These molecules make the female less attractive to other males, thus protecting her mate's sperm investment. Females have evolved the capacity to counteract this inhibition by ejecting the semen hydrocarbon (along with the rest of the remaining ejaculate) a few hours after mating. Although this ejection can temporarily restore the female's attractiveness, shortly thereafter another male pheromone, a seminal peptide, decreases the female's propensity to re-mate, thus continuing to protect the male's investment. Females use olfaction and taste sensing to select optimal egg-laying sites, integrating cues for the availability of food for her offspring, and the presence of other flies and of harmful species. We argue that taking into account evolutionary considerations such as sexual conflict, and the ecological conditions in which flies live, is helpful in understanding the role of highly species-specific pheromones and blends thereof, as well as an individual's response to the chemical cues in its environment

The role of cVA and the Odorant binding protein Lush in social and sexual behavior in <i>Drosophila melanogaster</i>:cVA and social behavior

Social living is beneficial because it allows conspecifics to interact in ways that increase their chances of survival and reproduction. A key mechanism underlying these benefits is the ability to recognize conspecifics; thus, allowing the production of coordinated social interactions. Identification of such individuals is often through chemical communication: the individuals’ pheromonal profile indicates their sex, species and even past experiences. However we know little about how the chemosensory system of conspecifics detects and how the nervous system processes this information. One of the best documented pheromonal detection mechanism is that of cis-Vaccenyl Acetate (cVA) made by male Drosophila melanogaster and transferred to females during mating. Sensing of cVA by males inhibits courtship behavior towards already mated females. Sensing of cVA on other males also inhibits courtship and increases aggression. In this hybrid review/research article, we discuss the pheromonal system of Drosophila putting an emphasis on the molecular and cellular mechanisms involved in cVA sensing by the olfactory system, perception by the nervous system and ultimately the regulation of social interactions. The behavioral effect of cVA is context- as well as experience-dependent leading us to conclude that cVA plays a modulatory role in regulating social interactions rather than being a recognition pheromone. We also provide new behavioral data on the function of the Odorant Binding Protein Lush, which binds cVA in olfactory sensilla and help sensing this chemical. Our data indicate that lush may be involved in the sensing of additional pheromones to cVA and suggest the existence of a lush-independent cVA detecting system. Interpretation of our data in the light of our current knowledge about pheromonal recognition in Drosophila indicates that this system is still incompletely understood

Lack of alignment across yeast-dependent life-history traits may limit <i>Drosophila melanogaster</i> dietary specialization

Heterogeneity in food resources is a major driver of local adaptation and speciation. Dietary specialization typically involves multiple life-history traits and may thus be limited by the extent to which these traits adapt in concert. Here, we use Drosophila melanogaster, representing an intermediate state in the generalist-specialist continuum, to explore the scope for dietary specialization. D. melanogaster has a close association with yeast, an essential but heterogeneous food resource. We quantify how different D. melanogaster strains from around the globe respond to different yeast species, across multiple yeast-dependent life-history traits including feeding, mating, egg-laying, egg development and survival. We find that D. melanogaster strains respond to different yeast species in different ways, indicating distinct fly strain-yeast interactions. However, we detect no evidence for trade-offs: fly performance tends to be positively rather than negatively correlated across yeast species. We also find that the responses to different yeast species are not aligned across traits: different life-history traits are maximized on different yeast species. Finally, we confirm that D. melanogaster is a resource generalist: it can grow, reproduce and survive on all the yeast species we tested. Together, these findings provide a possible explanation for the limited extent of dietary specialization in D. melanogaster.</p

<i>Drosophila melanogaster</i> females restore their attractiveness after mating by removing male anti-aphrodisiac pheromones

Males from many species ensure paternity by preventing their mates from copulating with other males. One mate-guarding strategy involves marking females with anti-aphrodisiac pheromones (AAPs), which reduces the females' attractiveness and dissuades other males from courting. Since females benefit from polyandry, sexual conflict theory predicts that females should develop mechanisms to counteract AAPs to achieve additional copulations, but no such mechanisms have been documented. Here we show that during copulation Drosophila melanogaster males transfer two AAPs: cis-Vaccenyl Acetate (cVA) to the females' reproductive tract, and 7-Tricosene (7-T) to the females' cuticle. A few hours after copulation, females actively eject cVA from their reproductive tract, which results in increased attractiveness and re-mating. Although 7-T remains on those females, we show that it is the combination of the two chemicals that reduces attractiveness. To our knowledge, female AAP ejection provides the first example of a female mechanism that counter-acts chemical mate-guarding

Divergent evolution of genetic sex determination mechanisms along environmental gradients

Sex determination (SD) is a crucial developmental process, but its molecular underpinnings are very diverse, both between and within species. SD mechanisms have traditionally been categorized as either genetic (GSD) or environmental (ESD), depending on the type of cue that triggers sexual differentiation. However, mixed systems, with both genetic and environmental components, are more prevalent than previously thought. Here, we show theoretically that environmental effects on expression levels of genes within SD regulatory mechanisms can easily trigger within-species evolutionary divergence of SD mechanisms. This may lead to the stable coexistence of multiple SD mechanisms and to spatial variation in the occurrence of different SD mechanisms along environmental gradients. We applied the model to the SD system of the housefly, a global species with world-wide latitudinal clines in the frequencies of different SD systems, and found that it correctly predicted these clines if specific genes in the housefly SD system were assumed to have temperature-dependent expression levels. We conclude that environmental sensitivity of gene regulatory networks may play an important role in diversification of SD mechanisms

Divergent evolution of genetic sex determination mechanisms along environmental gradients

Sex determination (SD) is a crucial developmental process, but its molecular underpinnings are very diverse, both between and within species. SD mechanisms have traditionally been categorized as either genetic or environmental SD, depending on the type of cue that triggers sexual differentiation. Mixed systems, in which SD is affected by genetic as well as environmental factors, are however more prevalent than previously thought. Such systems nonetheless remain understudied in the context of evolutionary stability and dynamics. We have developed a theoretical model to explore how environmental influences on SD genes can affect evolution of SD mechanisms. We found that environmental effects on expression levels of genes within SD regulatory mechanisms can easily trigger evolutionary divergence of SD mechanisms. This may lead to the stable coexistence of multiple SD mechanisms and to spatial variation in the occurrence of different SD mechanisms along environmental gradients. We applied the model to the SD system of the housefly, a global species with worldwide latitudinal clines in the frequencies of various SD systems, involving multiple different genes. We found that it correctly predicted these clines if specific genes in the housefly SD system were assumed to have temperature-dependent expression levels. We conclude that environmental sensitivity of gene regulatory networks may play an important role in diversification of SD mechanisms

Divergent evolution of genetic sex determination mechanisms along environmental gradients

Sex determination (SD) is a crucial developmental process, but its molecular underpinnings are very diverse, both between and within species. SD mechanisms have traditionally been categorized as either genetic or environmental SD, depending on the type of cue that triggers sexual differentiation. Mixed systems, in which SD is affected by genetic as well as environmental factors, are however more prevalent than previously thought. Such systems nonetheless remain understudied in the context of evolutionary stability and dynamics. We have developed a theoretical model to explore how environmental influences on SD genes can affect evolution of SD mechanisms. We found that environmental effects on expression levels of genes within SD regulatory mechanisms can easily trigger evolutionary divergence of SD mechanisms. This may lead to the stable coexistence of multiple SD mechanisms and to spatial variation in the occurrence of different SD mechanisms along environmental gradients. We applied the model to the SD system of the housefly, a global species with worldwide latitudinal clines in the frequencies of various SD systems, involving multiple different genes. We found that it correctly predicted these clines if specific genes in the housefly SD system were assumed to have temperature-dependent expression levels. We conclude that environmental sensitivity of gene regulatory networks may play an important role in diversification of SD mechanisms

Seven questions on the chemical ecology and neurogenetics of resource-mediated speciation

Adaptation to different environments can result in reproductive isolation between populations and the formation of new species. Food resources are among the most important environmental factors shaping local adaptation. The chemosensory system, the most ubiquitous sensory channel in the animal kingdom, not only detects food resources and their chemical composition, but also mediates sexual communication and reproductive isolation in many taxa. Chemosensory divergence may thus play a crucial role in resource-mediated adaptation and speciation. Understanding how the chemosensory system can facilitate resource-mediated ecological speciation requires integrating mechanistic studies of the chemosensory system with ecological studies, to link the genetics and physiology of chemosensory properties to divergent adaptation. In this review, we use examples of insect research to present seven key questions that can be used to understand how the chemosensory system can facilitate resource-mediated ecological speciation in consumer populations

Mating increases <i>Drosophila melanogaster</i> females' choosiness by reducing olfactory sensitivity to a male pheromone

Females that are highly selective when choosing a mate run the risk of remaining unmated or delaying commencing reproduction. Therefore, low female choosiness would be beneficial when males are rare but it would be maladaptive if males become more frequent. How can females resolve this issue? Polyandry would allow mating-status-dependent choosiness, with virgin females selecting their first mate with little selectivity and becoming choosier thereafter. This plasticity in choosiness would ensure timely acquisition of sperm and enable females to increase offspring quality during later mating. Here, we show that Drosophila melanogaster females display such mating-status-dependent choosiness by becoming more selective once mated and identify the underlying neurohormonal mechanism. Mating releases juvenile hormone, which desensitizes Or47b olfactory neurons to a pheromone produced by males, resulting in increased preference for pheromone-rich males. Besides providing a mechanism to a long-standing evolutionary prediction, these data suggest that intersexual selection in D. melanogaster, and possibly in all polyandrous, sperm-storing species, is mainly the domain of mated females since virgin females are less selective. Juvenile hormone influences behaviour by changing cue responsiveness across insects; the neurohormonal modulation of olfactory neurons uncovered in D. melanogaster provides an explicit mechanism for how this hormone modulates behavioural plasticity