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The Department of Entomology
The Robert H. Smith Faculty of Agriculture, Food and Environment
The Hebrew University of Jerusalem
P.O Box 12, Rehovot 76100, ISRAEL

Tel: 08-9489223 
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Email: orlytal@savion.huji.ac.il

Publications

2020
Levi-Zada, A. ; Levy, A. ; Rempoulakis, P. ; Fefer, D. ; Steiner, S. ; Gazit, Y. ; Nestel, D. ; Yuval, B. ; Byers, J. A. Diel rhythm of volatile emissions of males and females of the peach fruit fly Bactrocera zonata. Journal of Insect Physiology 2020, 120. Publisher's VersionAbstract
Fruit flies in the genus Bactrocera are among the most destructive insect pests of fruits and vegetables throughout the world. A number of studies have identified volatiles from fruit flies, but few reports have demonstrated behavioral effects or sensitivities of fly antennae to these compounds. We applied a recently developed method of automated headspace analysis using SPME (Solid Phase Microextraction) fibers and GC–MS (gas chromatography mass spectrometry), termed SSGA, to reveal volatiles specific to each sex of B. zonata that are emitted in a diel periodicity. The volatiles released primarily at dusk were identified by GC–MS and chemical syntheses as several spiroacetals, pyrazines, and ethyl esters. Solvent extraction of male rectal glands or airborne collections from each sex, followed by GC–MS, showed that certain of the volatiles increase or decrease in quantity sex-specifically with age of the flies. Electroantennographic (EAG) analysis of dose-response indicates differences in sensitivities of male and female antenna to the various volatiles. Our study provides a comprehensive analysis of the volatile chemicals produced and released by B. zonata and their antennal responses. The possible pheromone and semiochemical roles of the various volatiles released by each sex and the difficulties of establishing behavioral functions are discussed. © 2019 Elsevier Ltd
2019
Yuval, B. ; Lahuatte, P. ; Jose, P. A. ; Causton, C. E. ; Jurkevitch, E. ; Kouloussis, N. ; Ben-Yosef, M. Behavioral responses of the invasive fly Philornis downsi to stimuli from bacteria and yeast in the laboratory and the field in the Galapagos Islands. Insects 2019, 10. Publisher's VersionAbstract
Philornis downsi Dodge and Aitken (Diptera: Muscidae) is an avian parasitic fly that has invaded the Galapagos archipelago and exerts an onerous burden on populations of endemic land birds. As part of an ongoing effort to develop tools for the integrated management of this fly, our objective was to determine its long-and short-range responses to bacterial and fungal cues associated with adult P. downsi. We hypothesized that the bacterial and fungal communities would elicit attraction at distance through volatiles, and appetitive responses upon contact. Accordingly, we amplified bacteria from guts of adult field-caught flies and from bird feces, and yeasts from fermenting papaya juice (a known attractant of P. downsi), on selective growth media, and assayed the response of flies to these microbes or their exudates. In the field, we baited traps with bacteria or yeast and monitored adult fly attraction. In the laboratory, we used the proboscis extension response (PER) to determine the sensitivity of males and females to tarsal contact with bacteria or yeast. Long range trapping efforts yielded two female flies over 112 trap-nights (attracted by bacteria from bird feces and from the gut of adult flies). In the laboratory, tarsal contact with stimuli from gut bacteria elicited significantly more responses than did yeast stimuli. We discuss the significance of these findings in context with other studies in the field and identify targets for future work. © 2019 by the authors. Licensee MDPI, Basel, Switzerland.
Akami, M. ; Andongma, A. A. ; Zhengzhong, C. ; Nan, J. ; Khaeso, K. ; Jurkevitch, E. ; Niu, C. - Y. ; Yuval, B. Intestinal bacteria modulate the foraging behavior of the oriental fruit fly Bactrocera dorsalis (Diptera: Tephritidae). PLoS One 2019, 14, e0210109.Abstract
The gut microbiome of insects directly or indirectly affects the metabolism, immune status, sensory perception and feeding behavior of its host. Here, we examine the hypothesis that in the oriental fruit fly (Bactrocera dorsalis, Diptera: Tephritidae), the presence or absence of gut symbionts affects foraging behavior and nutrient ingestion. We offered protein-starved flies, symbiotic or aposymbiotic, a choice between diets containing all amino acids or only the non-essential ones. The different diets were presented in a foraging arena as drops that varied in their size and density, creating an imbalanced foraging environment. Suppressing the microbiome resulted in significant changes of the foraging behavior of both male and female flies. Aposymbiotic flies responded faster to the diets offered in experimental arenas, spent more time feeding, ingested more drops of food, and were constrained to feed on time-consuming patches (containing small drops of food), when these offered the full complement of amino acids. We discuss these results in the context of previous studies on the effect of the gut microbiome on host behavior, and suggest that these be extended to the life history dimension.
Jose, P. A. ; Ben-Yosef, M. ; Jurkevitch, E. ; Yuval, B. Symbiotic bacteria affect oviposition behavior in the olive fruit fly Bactrocera oleae. J Insect Physiol 2019, 117, 103917.Abstract
Microbial associations are widespread across the insects. In the olive fruit fly Bactrocera oleae (Diptera: Tephritidae), vertically transmitted gut symbionts contribute to larval development inside the olive host, and to adult nutrition. Nevertheless, their effect on behavioural decisions of adults is unknown. In this study, we show that symbiotic bacteria affect oviposition behaviour in B. oleae. We studied the effect of different fruits as hosts and different gut-bacteria as gut-symbionts on oviposition attempts and fly development in B. oleae. Untreated flies that had native gut-symbionts attempted oviposition significantly more times than axenic flies as well as flies treated with medfly-associated Pantoea or Klebsiella bacteria. Axenic flies provided with a diet containing the homogenized gut of symbiotic flies recovered the same number of oviposition attempts as their symbiotic counterparts. As for as the different hosts, green olives (unripe) and grapes were preferred while black olives (ripe) elicited the least number of oviposition attempts, with an interactive effect of host and bacterial treatments. It appears that both the host attributes and the native gut-symbionts drive oviposition preference towards green olives in B. oleae. Moreover, both bacterial treatments and hosts significantly affected the development of B. oleae larvae. Though grapes elicited as many oviposition attempts as green olives, they yielded no pupae. Taken together, our results suggest that the intimate association between B. oleae and their gut-microbes, extends beyond nutritional support to behaviour.
2017
Yuval, B. Symbiosis: Gut Bacteria Manipulate Host Behaviour. Current Biology 2017, 27, R746 - R747. Publisher's VersionAbstract
Summary Bacteria resident in the gut of Drosophila modify the fly’s innate chemosensory responses to nutritional stimuli. In effect, the gut microbiome compels the host to forage on food patches that favour particular assemblages of bacteria.
Ben-Yosef, M. ; Zaada, D. S. Y. ; Dudaniec, R. Y. ; Pasternak, Z. ; Jurkevitch, E. ; Smith, R. J. ; Causton, C. E. ; Lincango, M. P. ; Tobe, S. S. ; Mitchell, J. G. ; et al. Host-specific associations affect the microbiome of Philornis downsi, an introduced parasite to the Galápagos Islands. Mol Ecol 2017, 26, 4644-4656.Abstract
The composition and diversity of bacteria forming the microbiome of parasitic organisms have implications for differential host pathogenicity and host-parasite co-evolutionary interactions. The microbiome of pathogens can therefore have consequences that are relevant for managing disease prevalence and impact on affected hosts. Here, we investigate the microbiome of an invasive parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, where it poses extinction threat to Darwin's finches and other land birds. Larvae infest nests of Darwin's finches and consume blood and tissue of developing nestlings, and have severe mortality impacts. Using 16s rRNA sequencing data, we characterize the bacterial microbiota associated with P. downsi adults and larvae sourced from four finch host species, inhabiting two islands and representing two ecologically distinct groups. We show that larval and adult microbiomes are dominated by the phyla Proteobacteria and Firmicutes, which significantly differ between life stages in their distributions. Additionally, bacterial community structure significantly differed between larvae retrieved from strictly insectivorous warbler finches (Certhidea olivacea) and those parasitizing hosts with broader dietary preferences (ground and tree finches, Geospiza and Camarhynchus spp., respectively). Finally, we found no spatial effects on the larval microbiome, as larvae feeding on the same host (ground finches) harboured similar microbiomes across islands. Our results suggest that the microbiome of P. downsi changes during its development, according to dietary composition or nutritional needs, and is significantly affected by host-related factors during the larval stage. Unravelling the ecological significance of bacteria for this parasite will contribute to the development of novel, effective control strategies.
Pavlidi, N. ; Gioti, A. ; Wybouw, N. ; Dermauw, W. ; Ben-Yosef, M. ; Yuval, B. ; Jurkevitch, E. ; Kampouraki, A. ; Van Leeuwen, T. ; Vontas, J. Transcriptomic responses of the olive fruit fly Bactrocera oleae and its symbiont Candidatus Erwinia dacicola to olive feeding. Sci Rep 2017, 7 42633.Abstract
The olive fruit fly, Bactrocera oleae, is the most destructive pest of olive orchards worldwide. The monophagous larva has the unique capability of feeding on olive mesocarp, coping with high levels of phenolic compounds and utilizing non-hydrolyzed proteins present, particularly in the unripe, green olives. On the molecular level, the interaction between B. oleae and olives has not been investigated as yet. Nevertheless, it has been associated with the gut obligate symbiotic bacterium Candidatus Erwinia dacicola. Here, we used a B.oleae microarray to analyze the gene expression of larvae during their development in artificial diet, unripe (green) and ripe (black) olives. The expression profiles of Ca. E. dacicola were analyzed in parallel, using the Illumina platform. Several genes were found overexpressed in the olive fly larvae when feeding in green olives. Among these, a number of genes encoding detoxification and digestive enzymes, indicating a potential association with the ability of B. oleae to cope with green olives. In addition, a number of biological processes seem to be activated in Ca. E. dacicola during the development of larvae in olives, with the most notable being the activation of amino-acid metabolism.