Recent Publications
Divergent sensory investment mirrors potential speciation via niche partitioning across Drosophila
The examination of phylogenetic and phenotypic characteristics of the nervous system, such as behavior and neuroanatomy, can be utilized as a means to assess speciation. Recent studies have proposed a fundamental tradeoff between two sensory organs, the eye and the antenna. However, the identification of ecological mechanisms for this observed tradeoff have not been firmly established. Our current study examines several monophyletic species within the obscura group, and asserts that despite their close relatedness and overlapping ecology, they deviate strongly in both visual and olfactory investment. We contend that both courtship and microhabitat preferences support the observed inverse variation in these sensory traits. Here, this variation in visual and olfactory investment seems to provide relaxed competition, a process by which similar species can use a shared environment differently and in ways that help them coexist. Moreover, that behavioral separation according to light gradients occurs first, and subsequently, courtship deviations arise.
Variable dependency on associated yeast communities influences host range in Drosophila species
The tight association between yeast metabolites and the attraction of fly species provides key evolutionary innovations that generate immense diversity within the genus Drosophila. Why and how changes in Drosophila niche preferences occur, and what role yeasts play in species specialization, is still largely unknown. Here, we analyze adult preference and larval development across three species of Drosophila as well as niche modifications through joint efforts by both insect and yeast. In general, we found that niche specialization is more a result of larval constraints than adult oviposition choice. We also determined that different life stages of fly development vary in their respective yeast preference, which may reduce cross‐generational competition for resources.
Plant-based natural product chemistry for integrated pest management of Drosophila suzukii
In a new direction of study, we present an investigation of plant-based chemistry, where we search for natural compounds that are structurally similar to known olfactory cues from parasitoid wasps that in turn are well-described ovipositional avoidance cues for many Drosophila species. Here we test 11 plant species across two plant genera, Nepeta and Actinidia, and while we find iridoid compounds in both, only those odorants from Actinidia are noted to be detected by the insect antenna, and in addition, found to be behaviorally active. Moreover, the Actinidia extracts resulted in oviposition avoidance when they were added to fruit samples in the laboratory. Thus we propose the possible efficacy of these plants or their extracted chemistry as a novel means for establishing a cost-effective integrated pest management strategy towards the control of this pest fly.
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Inverse resource allocation between vision and olfaction across the genus Drosophila
Divergent populations across different environments are exposed to critical sensory information related to locating a host or mate, as well as avoiding predators and pathogens. These sensory signals generate evolutionary changes in neuroanatomy and behavior; however, few studies have investigated patterns of neural architecture that occur between sensory systems, or that occur within large groups of closely-related organisms. Here we examine 62 species within the genus Drosophila, and describe an inverse resource allocation between vision and olfaction, which we consistently observe at the periphery, within the brain, as well as during larval development. This sensory variation was noted across the entire genus, and appears to represent repeated, independent evolutionary events, where one sensory modality is consistently selected for at the expense of the other. Moreover, we provide evidence of a developmental genetic constraint through the sharing of a single larval structure, the eye-antennal imaginal disc. In addition, we examine the ecological implications of visual or olfactory bias, including the potential impact on host-navigation and courtship.
Gut microbiota affects development and olfactory behavior in Drosophila melanogaster
It has been shown that gut microbes are very important for the behavior and development of Drosophila, as the beneficial microbes are involved in the identification of suitable feeding and oviposition places. However, in what way these associated gut microbes influence the fitness-related behaviors of Drosophila melanogaster remains unclear. Here we show that D. melanogaster exhibits different behavioral preferences towards gut microbes. Both adults and larvae were attracted by the headspace of Saccharomyces cerevisiae and Lactobacillus plantarum, but were repelled by Acetobacter malorum in behavioral assays, indicating an olfactory mechanism involved in these preference behaviors. By experimentally manipulating the microbiota of the flies, we found that flies did not strive for a diverse microbiome by e.g. increasing their preference towards gut microbes that they had not experienced previously. Thus our study provides a better understanding of how gut microbes affect insect behavior and development, and offers an ecological rationale for preferences of flies for different microbes in their natural environment.
Evaluation of the DREAM technique for a high-throughput deorphanization of chemosensory receptors in Drosophila
Here we tested the potential of the DREAM technique (Deorphanization of Receptors based on Expression Alterations in mRNA levels) for high-throughput identification of chemosensory receptors across novel insect species by first establishing the results in D. melanogaster as a known model. We confirmed that in some cases that the exposure of a chemosensory receptor to high concentration of its best ligand does lead to measureable alterations in mRNA levels. However, unlike in mammals, we found several cases where either confirmed ligands did not induce alterations in mRNA levels of the corresponding chemosensory receptors, or where gene transcript-levels were altered even though there is no evidence for a ligand-receptors interaction. Hence, there are severe limitations to the suitability of the DREAM technique for deorphanization as a general tool to characterize olfactory receptors in new insects, and we describe ways this technique could be optimized to be more reliable and accurate.
LINK TO PUBLICATION Koerte et al. (2018) Front. Mol. Neurosci.
Pathogenic bacteria enhance dispersal through alteration of Drosophila social communication
Pathogens and parasites can manipulate their hosts to optimize their own fitness. For instance, bacterial pathogens have been shown to affect their host plants’ volatile and non-volatile metabolites, which results in increased attraction of insect vectors to the plant, and, hence, to increased pathogen dispersal. Behavioral manipulation by parasites has also been shown for mice, snails and zebrafish as well as for insects. Here we show that infection by pathogenic bacteria alters the social communication system of Drosophila melanogaster. More specifically, infected flies and their frass emit dramatically increased amounts of fly odors, including the aggregation pheromones methyl laurate, methyl myristate, and methyl palmitate, attracting healthy flies, which in turn become infected and further enhance pathogen dispersal. Thus, olfactory cues for attraction and aggregation are vulnerable to pathogenic manipulation, and we show that the alteration of social pheromones can be beneficial to the microbe while detrimental to the insect host.
https://doi.org/10.1038/s41467-017-00334-9
Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects
Flying insects are well-known for airborne odor tracking, and evolved diverse chemoreceptors. While ionotropic receptors (IRs) are found across Protostomes, insect odorant receptors (ORs) have only been identified in winged insects. We therefore hypothesize that the unique signal transduction of ORs offers an advantage for odor localization in flight. Using Drosophila, we find expression and increased activity of the intracellular signaling protein, PKC, in antennal sensilla following odor stimulation. Odor stimulation also enhances phosphorylation of the OR coreceptor, Orco, in vitro, while site directed mutation of Orco or mutations in PKC subtypes reduces sensitivity and dynamic ranges of OR-expressing neurons in vivo, but not IRs. We ultimately show that these mutations reduce competence for odor localization of flies in flight. We conclude that intracellular regulation of OR sensitivity is necessary for efficient odor localization, which suggests a mechanistic advantage for the evolution of the OR complex in flying insects.
Adult frass provides a pheromone signature for Drosophila feeding and aggregation
In this study, we demonstrate that Drosophila adults are able to recruit additional flies to a food source by covering the exposed surface area with fecal spots, and that this recruitment is mediated via olfactory receptors (Ors). Analyses of the deposited frass material demonstrates that frass contains several previously studied pheromone components, such as methyl laurate (ML), methyl myristate (MM), methyl palmitate (MP), and 11-cis-vaccenyl acetate (cVA), in addition to several cuticular hydrocarbons (CHCs) that are known to be behaviorally active. Moreover, this study also demonstrates that adult feeding is increased in the presence of frass, although it appears that Ors are less likely to mediate this phenomenon. In summary, the frass deposited by the fly onto the fruit provides both pheromone and CHC cues that lead to increased feeding and aggregation in Drosophila. This research is the first step in examining Drosophila frass as an important chemical signature that provides information about both the sex and the species of the fly that generated the fecal spots.
Hawkmoths evaluate scenting flowers with the tip of their proboscis
Pollination by insects is essential to many ecosystems. Previously, we have shown that floral scent is important to mediate pollen transfer between plants (Kessler et al., 2015). Yet, the mechanisms by which pollinators evaluate volatiles of single flowers remained unclear. Here, Nicotiana attenuata plants, in which floral volatiles have been genetically silenced and its hawkmoth pollinator, Manduca sexta, were used in semi-natural tent and wind-tunnel assays to explore the function of floral scent. We found that floral scent functions to increase the fitness of individual flowers not only by increasing detectability but also by enhancing the pollinator's foraging efforts. Combining proboscis choice tests with neurophysiological, anatomical and molecular analyses we show that this effect is governed by newly discovered olfactory neurons on the tip of the moth's proboscis. With the tip of their tongue, pollinators assess the advertisement of individual flowers, an ability essential for maintaining this important ecosystem service.
Pheromones mediating copulation and attraction in Drosophila
Here we show that Or47b-and Or88a-expressing olfactory sensory neurons (OSNs) detect the fly-produced odorants methyl laurate (ML), methyl myristate, and methyl palmitate. Fruitless (fruM)-positive Or47b-expressing OSNs detect ML exclusively, and Or47b- and Or47b-expressing OSNs are required for optimal male copulation behavior. In addition, activation of Or47b-expressing OSNs in the male is sufficient to provide a competitive mating advantage. We further find that the vigorous male courtship displayed toward oenocyte-less flies is attributed to an oenocyte-independent sustained production of the Or47b ligand, ML. Beyond the OSN level, information regarding the three fly odorants is transferred from the antennal lobe to higher brain centers in two dedicated neural lines. Finally, we find that both Or47b- and Or88a-based systems and their ligands are remarkably conserved over a number of drosophilid species.
Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit
It has been demonstrated that Drosophila suzukii is capable of attacking ripening fruit, making it a unique species within a fly family named for their attraction towards the fermentation products associated with rotten fruits, vinegar, and yeast. It also has been hypothesized that D. suzukii is more attracted to the volatiles associated with the earlier ripening stages of fruit development, and in turn, that D. suzukii is less attracted to fermented food resources, especially when compared with D. melanogaster. Here, we demonstrate that D. suzukii and its close relative D. biarmipes are in fact more sensitive to volatiles associated with the fruit-ripening process; however, in choice-assays, both spotted-wing species are more attracted to fermented fruit than to earlier stages of fruit development, which is similar to the behavioral preferences of D. melanogaster, and thus, fruit developmental stage alone does not explain the ecological niche observed for D. suzukii. In contrast, we show that both D. suzukii and D. biarmipes are more attracted to leaf odors than D. melanogaster in behavioral trials. For D. suzukii, this differential behavioral preference towards leaves appears to be linked to β-cyclocitral, a volatile isoprenoid that we show is most likely a novel ligand.
