Wild African Drosophila melanogaster are seasonal specialists on marula fruits

Although the vinegar fly Drosophila melanogaster isarguably the most studied organism on the planet,fundamental aspects of this species’ natural ecologyhave remained enigmatic [1]. We have here investigateda wild population of D. melanogaster from amopane forest in Zimbabwe. We find that these fliesare closely associated with marula fruit (Sclerocaryabirrea) and propose that this seasonally abundantand predominantly Southern African fruit is a keyancestral host of D. melanogaster. Moreover, whenfruiting, marula is nearly exclusively used byD. melanogaster, suggesting that these forest-dwellingD. melanogaster are seasonal specialists, in asimilar manner to, e.g., Drosophila erecta on screwpine cones [2]. We further demonstrate that themain chemicals released by marula activate odorantreceptors that mediate species-specific host choice(Or22a) [3, 4] and oviposition site selection (Or19a)[5]. The Or22a-expressing neurons—ab3A—respondstrongly to the marula ester ethyl isovalerate, a volatilerarely encountered in high amounts in other fruit.We also show that Or22a differs among African populationssampled from a wide range of habitats, inline with a function associated with host fruit usage.Flies from Southern Africa, most of which carry adistinct allele at the Or22a/Or22b locus, have ab3Aneurons that are more sensitive to ethyl isovaleratethan, e.g., European flies. Finally, we discuss thepossibility that marula, which is also a culturallyand nutritionally important resource to humans,may have helped the transition to commensalism inD. melanogaster

Drosophila Sensory Neuroethology

Animals, like humans, need to perceive their surroundings via their senses in order to make sensible behavioral decisions, reproduce successfully, and survive. Animals are equipped with audition, vision, thermosensation, hygrosensation, mechanosensation, magnetoception, gustation, and olfaction, which detects physical and chemical changes in their habitats. Among these senses, olfaction is likely the most ancient sensory modality. Insects, the most abundant and successful group of the animal kingdom, predominantly use olfaction to find food, mates, breeding sites, and to avoid dangers. Moreover, hygrosensation is vital for insects to find a suitable habitat and to avoid risks of dehydration. Our understanding of the molecular, neuronal, and morphological organization of the insect olfactory system is today substantial, in large parts thanks to Drosophila melanogaster (vinegar fly) and the wealth of sophisticated genetic tools available in this classic model system. Our knowledge regarding the functional and molecular basis of insect hygrosensation, is, however, limited. In this thesis, I show that the vinegar fly olfactory system do not detect odor molecules randomly, but capture and process specific odors associated with needs and dangers. I demonstrate how the olfactory system cope with toxic and harmful matters in the natural habitat and I identify an olfactory circuit that mediates repellency towards phenol, which is produced by pathogenic bacteria, predominantly present in carnivore feces. Furthermore, I show that flies have an innate and species-specific ability to find suitable humidity levels, related to their native habitat. Vinegar flies can sense humidity changes in their environment through a trio of ionotropic receptors expressed in the sacculus of the antennae. Although D. melanogaster is known as a generalist, I show that wild populations of D. melanogaster from a mopane forest within the potential ancestral habitat have a strong breeding preference towards marula fruit. This fruit is seasonally abundant, native to Southern Africa, and is presumably the ancestral host of the vinegar fly. I also argue that marula drove the D. melanogaster to become a human commensal. In summary, the research presented in my thesis enhances our understanding of how the olfactory system operates, the behavior of wild flies, and introduces the genetic and neural basis underlying humidity sensation in insects. These findings might lead us to better strategies for controlling insect pests, as well as human disease vectors

The chemical ecology of the fly.

Not only is the sense of smell of pivotal importance to most animals but also serves as a significant model system in biological research. In recent years, great strides in our understanding of how the olfactory system is organized and operates have been made. Instrumental in these efforts has been work performed in Drosophila melanogaster. In spite of the wealth of information gathered, it remains unclear how the fly's olfactory system is used to decode the chemical environment. Here we describe recent findings on the chemical ecology of the fly and speculate on possible functions of the volatile chemicals that flies detect. We argue that for many of the fly's olfactory chemoreceptors, distinct and ecologically relevant functions can be identified

Fecal-Derived Phenol Induces Egg-Laying Aversion in Drosophila

Feces is an abundant, rich source of energy, utilized by a myriad of organisms, not least by members of the order Diptera, i.e., flies. How Drosophila melanogaster reacts to fecal matter remains unclear. Here, we examined oviposition behavior toward a range of fecal samples from mammals native to the putative Southeast African homeland of the fly. We show that D. melanogaster display a strong oviposition aversion toward feces from carnivorous mammals but indifference or even attraction toward herbivore dung. We identify a set of four predictor volatiles, which can be used to differentiate fecal from non-fecal matter, as well as separate carnivore from herbivore feces. Of these volatiles, phenol—indicative of carnivore feces—confers egg-laying aversion and is detected by a single class of sensory neurons expressing Or46a. The Or46a-expressing neurons are necessary and sufficient for oviposition site aversion. We further demonstrate that carnivore feces—unlike herbivore dung—contain a high rate of pathogenic bacteria taxa. These harmful bacteria produce phenol from L-tyrosine, an amino acid specifically enriched in high protein diets, such as consumed by carnivores. Finally, we demonstrate that carnivore feces, as well as phenol, is also avoided by a ball-rolling species of dung beetle, suggesting that phenol is a widespread avoidance signal because of its association with pathogenic bacteria

Humidity Sensing in Drosophila

Environmental humidity influences the fitness and geographic distribution of all animals [1]. Insects in particular use humidity cues to navigate the environment, and previous work suggests the existence of specific sensory mechanisms to detect favorable humidity ranges [2-5]. Yet, the molecular and cellular basis of humidity sensing (hygrosensation) remains poorly understood. Here we describe genes and neurons necessary for hygrosensation in the vinegar fly Drosophila melanogaster. We find that members of the Drosophila genus display species-specific humidity preferences related to conditions in their native habitats. Using a simple behavioral assay, we find that the ionotropic receptors IR40a, IR93a, and IR25a are all required for humidity preference in D. melanogaster. Yet, whereas IR40a is selectively required for hygrosensory responses, IR93a and IR25a mediate both humidity and temperature preference. Consistent with this, the expression of IR93a and IR25a includes thermosensory neurons of the arista. In contrast, IR40a is excluded from the arista but is expressed (and required) in specialized neurons innervating pore-less sensilla of the sacculus, a unique invagination of the third antennal segment. Indeed, calcium imaging showed that IR40a neurons directly respond to changes in humidity, and IR40a knockdown or IR93a mutation reduced their responses to stimuli. Taken together, our results suggest that the preference for a specific humidity range depends on specialized sacculus neurons, and that the processing of environmental humidity can happen largely in parallel to that of temperature

Recurrant collection of Drosophila melanogaster from wild African environments and genomic insights into species history

A long-standing enigma concerns the geographic and ecological origins of the intensively studied vinegar fly, Drosophilamelanogaster. This globally distributed human commensal is thought to originate from sub-Saharan Africa, yet untilrecently, it had never been reported from undisturbed wilderness environments that could reflect its precommensalniche. Here, we document the collection of 288 D. melanogaster individuals from multiple African wilderness areas inZambia, Zimbabwe, and Namibia. The presence of D. melanogaster in these remote woodland environments is consistentwith an ancestral range in southern-central Africa, as opposed to equatorial regions. After sequencing the genomes of 17wilderness-collected flies collected from Kafue National Park in Zambia, we found reduced genetic diversity relative totown populations, elevated chromosomal inversion frequencies, and strong differences at specific genes including knowninsecticide targets. Combining these genomes with existing data, we probed the history of this species’ geographicexpansion. Demographic estimates indicated that expansion from southern-central Africa began 10,000 years ago,with a Saharan crossing soon after, but expansion from the Middle East into Europe did not begin until roughly 1,400years ago. This improved model of demographic history will provide an important resource for future evolutionary andgenomic studies of this key model organism. Our findings add context to the history of D. melanogaster, while openingthe door for future studies on the biological basis of adaptation to human environments