Pathogenic bacteria enhance dispersal through alteration of Drosophila social communication

Keesey, Ian W.; Koerte, Sarah; Khallaf, Mohammed A.; Retzke, Tom; Guillou, Aurélien; Große-Wilde, Ewald; Buchon, Nicolas; Knaden, Markus; Hansson, Bill S.

doi:10.1038/s41467-017-00334-9

Cited by 58 publications

(64 citation statements)

References 56 publications

(84 reference statements)

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“…Females were used from all species, and flies were between 2 and 7 days post-eclosion. An odor panel of 80 compounds was selected based on previous literature 10,11,18,22,61 , and was used to screen all OSNs across the antenna and palps of each examined species. In addition, when this odor screen failed to identify any strong ligands, we also utilized gaschromatography single-sensillum recordings (GC-SSR).…”

Section: Chemical Stimuli and Single Sensillum Recordingsmentioning

confidence: 99%

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Keesey

Zhang

Depetris-Chauvin

et al. 2019

Preprint

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Comparative analysis of multiple genomes has been used extensively to examine the evolution of chemosensory receptors across the genus Drosophila. However, few studies have delved into functional characteristics, as most have relied exclusively on genomic data alone, especially for non-model species. In order to increase our understanding of olfactory evolution, we have generated a comprehensive assessment of the olfactory functions associated with the antenna and palps for Drosophila suzukii as well as several other members of the subgenus Sophophora, thus creating a functional olfactory landscape across a total of 20 species. Here we identify and describe several common elements of evolution, including consistent changes in ligand spectra as well as relative receptor abundance, which appear heavily correlated with the known phylogeny. We also combine our functional ligand data with protein orthologue alignments to provide a high-throughput evolutionary assessment and predictive model, where we begin to examine the underlying mechanisms of evolutionary changes utilizing both genetics and odorant binding affinities. In addition, we document that only a few receptors frequently vary between species, and we evaluate the justifications for evolution to reoccur repeatedly within only this small subset of available olfactory sensory neurons.

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Section: Chemical Stimuli and Single Sensillum Recordingsmentioning

confidence: 99%

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Keesey

Zhang

Depetris-Chauvin

et al. 2019

Preprint

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“…Gut microbiomes play important roles in different physiological processes of their hosts, such as nutrition (Wong et al, 2014;Newell and Douglas, 2014;Tefit and Leulier, 2017;Leitão-Gonçalves et al, 2017), development (Ridley et al, 2012;Shin et al, 2011;Storelli et al, 2011;Tefit and Leulier, 2017), longevity (Guo et al, 2014;Clark et al, 2015), immunity (Sansone et al, 2015) and disease avoidance (Van Nood et al, 2013;Zhang et al, 2015). The fruit fly, Drosophila melanogaster, has been largely used to study host-microbe interactions related to innate immunity and pathogenic association (Lemaitre and Hoffmann, 2007;Keesey et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…The environmental microbes that flies have been exposed to as larvae and adults not only drive the composition of the flies' gut microbiome (Chandler et al, 2011), but can also affect the flies' behaviors, such as oviposition (Tefit and Leulier, 2017) or foraging (Wong et al, 2017;Leitão-Gonçalves et al, 2017;Keesey et al, 2017). Furthermore, Drosophila larvae and adults can be attracted by odors emanating from food patches that have been previously used by larvae (Durisko and Dukas, 2013;Durisko et al, 2014) and a study performed with axenic Drosophila revealed that at least some of these attractants are produced by the larval gut bacteria (Venu et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Gut microbiota affects development and olfactory behavior in Drosophila melanogaster

Qiao

Keesey

Hansson

et al. 2019

Journal of Experimental Biology

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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 egg-laying locations. 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 volatile compounds of Saccharomyces cerevisiae and Lactobacillus plantarum, but were repelled by Acetobacter malorum in behavioral assays, indicating that an olfactory mechanism is involved in these preference behaviors. While the attraction to yeast was governed by olfactory sensory neurons expressing the odorant co-receptor Orco, the observed behaviors towards the other microbes were retained in flies lacking this co-receptor. By experimentally manipulating the microbiota of the flies, we found that flies did not strive for a diverse microbiome by increasing their preference towards gut microbes that they had not experienced previously. Instead, in some cases, the flies even increased preference for the microbes on which they were reared. Furthermore, exposing Drosophila larvae to all three microbes promoted Drosophila development, while exposure to only S. cerevisiae and A. malorum resulted in the development of larger ovaries and in increased egg numbers in an oviposition assay. 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. The effect of gut microbiome on behavioral preference of fliesAfter showing that the flies become attracted to two of the microbe types and that all microbes positively affect the flies' oviposition 3

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“…The flatworm Leucochloridium paradoxum for instance modifies the eye stalks of snails to resemble caterpillars, which prompts birds to attack the eyes, thus allowing the flatworm to be transmitted to its primary host (39). Furthermore, the bacterial pathogen Pseudomonas entomophila triggers the release of aggregation pheromones from infected Drosophila melanogaster , which attracts healthy flies and thus enhances pathogen dispersal (14). We show that entomopathogenic nematodes can use volatile such as BHT to attract healthy rootworm larvae in the soil.…”

Section: Discussionmentioning

confidence: 99%

“…involving a single host) can facilitate transmission from exploited hosts to new healthy hosts is less well established (13). Recent studies show that insect bacterial pathogens can induce to changes in volatile emissions in infected individuals, which results in the attraction of non-infected individuals (14). Whether predators, parasitoids and multicellular parasites with direct life cycles can use volatiles to attract additional hosts or prey remains to be determined.…”

Section: Introductionmentioning

confidence: 99%

Entomopathogenic nematodes increase predation success by inducing specific cadaver volatiles that attract healthy herbivores

Zhang

Machado

Doan

et al. 2018

Preprint

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14Herbivore natural enemies, including predators, parasitoids and parasites, protect plants by 15 regulating herbivore populations. Some parasites can increase their transmission efficiency by 16 manipulating host behavior. Whether natural enemies can manipulate herbivore behavior to 17 increase top-down control, however, is unknown. Here, we investigate if and how the 18 entomopathogenic nematode Heterorhabditis bacteriophora, an important biocontrol agent, 19 modulates the behavior of the western corn rootworm, Diabrotica virgifera virgifera, a major 20 maize pest, and how these behavioral changes affect the capacity of the nematode to control the 21 rootworm. We found that healthy rootworm larvae are attracted to nematode-infected cadavers 22 shortly before the emergence of the next generation of nematodes. Nematode-infected rootworms 23 release distinct volatile bouquets, including butylated hydroxytoluene (BHT), which attracts 24 rootworms to infected cadavers. In a soil setting, BHT attracts rootworms and reduces nematode 25 resistance, resulting in increased infection rates and rootworm mortality as well as increased 26 nematode reproductive success. Five out of seven tested insect species were found to be attracted 27 to nematode-infected conspecifics, suggesting that attraction of healthy hosts to nematode-infected 28 cadavers is widespread. This study reveals a new facet of the biology of entomopathogenic 29 nematodes that increases their capacity to control a major root pest by increasing the probability of 30 host encounters. 31 Keywords: Belowground tritrophic interactions, entomopathogenic nematodes, prey attraction, 32 parasitism strategies, butylated hydroxytoluene 33 34Herbivore natural enemies such as predators, parasites and parasitoids play a key role in terrestrial 35 ecosystems by reducing herbivore abundance (1). Biological control relies on this form of top-36 down control to protect crops from herbivores (2). In order to exert their effects, herbivore natural 37 enemies need to make contact with their hosts. Natural enemies have evolved various behavioral 38 strategies to maximize their chance to encounter herbivores (3-6). Predators and parasitoids for 39 instance can use herbivore-induced plant volatiles to locate herbivores (7). Herbivores on the other 40 hand can detect and actively avoid contact with natural enemies (8). The interplay between 41 behavioral adaptations of herbivores and natural enemies is likely to be an important determinant 42 for the success of herbivore natural enemies and their capacity to suppress herbivore pests. 43A key step in the life of many herbivore natural enemies is the acquisition of new hosts once the 44 old host is exploited. Predators and parasitoids acquire new hosts by hunting, ambushing and 45 trapping them. Parasites with indirect life cycles can also facilitate the transfer to new hosts through 46 host manipulation strategies, including changes in color, smell and behavior of their current hosts 47 to attract alternate hosts (9-12). How p...

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Pathogenic bacteria enhance dispersal through alteration of Drosophila social communication

Cited by 58 publications

References 56 publications

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Evolution of a pest: towards the complete neuroethology of Drosophila suzukii and the subgenus Sophophora

Gut microbiota affects development and olfactory behavior in Drosophila melanogaster

Entomopathogenic nematodes increase predation success by inducing specific cadaver volatiles that attract healthy herbivores

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