Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila

Program in Biological Sciences, University of California, San Francisco, CA 94143-2822, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.81). 07/2009; 106(27):11352-7. DOI: 10.1073/pnas.0901419106
Source: PubMed

ABSTRACT Selection of appropriate oviposition sites is essential for progeny survival and fitness in generalist insect species, such as Drosophila melanogaster, yet little is known about the mechanisms regulating how environmental conditions and innate adult preferences are evaluated and balanced to yield the final substrate choice for egg-deposition. Female D. melanogaster are attracted to food containing acetic acid (AA) as an oviposition substrate. However, our observations reveal that this egg-laying preference is a complex process, as it directly opposes an otherwise strong, default behavior of positional avoidance for the same food. We show that 2 distinct sensory modalities detect AA. Attraction to AA-containing food for the purpose of egg-laying relies on the gustatory system, while positional repulsion depends primarily on the olfactory system. Similarly, distinct central brain regions are involved in AA attraction and repulsion. Given this unique situation, in which a single environmental stimulus yields 2 opposing behavioral outputs, we propose that the interaction of egg-laying attraction and positional aversion for AA provides a powerful model for studying how organisms balance competing behavioral drives and integrate signals involved in choice-like processes.

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    ABSTRACT: Insects encounter a vast repertoire of chemicals in their natural environment, which can signal positive stimuli like the presence of a food source, a potential mate, or a suitable oviposition site as well as negative stimuli such as competitors, predators, or toxic substances reflecting danger. The presence of specialized chemoreceptors like taste and olfactory receptors allows animals to detect chemicals at short and long distances and accordingly, trigger proper behaviors toward these stimuli. Since the first description of olfactory and taste receptors in Drosophila melanogaster 15 years ago, our knowledge on the identity, properties, and function of specific chemoreceptors has increased exponentially. In the last years, multidisciplinary approaches combining genetic tools with electrophysiological techniques, behavioral recording, evolutionary analysis, and chemical ecology studies are shedding light on our understanding on the ecological relevance of specific chemoreceptors for the survival of Drosophila in their natural environment. In this review we discuss the current knowledge on chemoreceptors of both the olfactory and taste systems of the fruitfly. We focus on the relevance of particular receptors for the detection of ecologically relevant cues such as pheromones, food sources, and toxic compounds, and we comment on the behavioral changes that the detection of these chemicals induce in the fly. In particular, we give an updated outlook of the chemical communication displayed during one of the most important behaviors for fly survival, the courtship behavior. Finally, the ecological relevance of specific chemicals can vary depending on the niche occupied by the individual. In that regard, in this review we also highlight the contrast between adult and larval systems and we propose that these differences could reflect distinctive requirements depending on the change of ecological niche occupied by Drosophila along its life cycle.
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    ABSTRACT: ABSTRACT Oviposition site-selection in insects is mediated through innate recognition templates (IRTs) tuned to specific chemical cues. These cues aid gravid insects in choosing suitable oviposition sites and may even enhance the fitness of their offspring by warding off predators and parasitoids. However, studies on the evolution of oviposition site-selection and cues instigating oviposition in domesticated insects remain elusive. Using the interaction between the silkmoth, Bombyx mori, and its host plant mulberry, Morus alba, as a model system, we demonstrate that centuries of domestication of silkmoth has not impaired its oviposition site-selection function. Silkmoths significantly preferred mulberry leaves to filter paper as oviposition sites. Oviposition assays with filter paper, filter paper treated with leaf volatiles and leaf alone proved that surface texture was not a significant criterion for oviposition site-selection, but volatile cues were. Oviposition assays with electrophysiologically active compounds from mulberry revealed that two of the volatiles, valencene and α-humulene, aided moths in choosing suitable oviposition sites and enhanced egg-laying significantly. Moreover, we show that generalist egg-parasitoids are strongly repelled by valencene and α-humulene. Our results demonstrate that IRTs tuned to cues that aid crucial functions like oviposition site-selection are less likely to be impaired even after centuries of domestication.
    Scientific Reports 11/2014; 12/2014. DOI:10.1038/srep07472 · 5.08 Impact Factor
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    ABSTRACT: Drosophila melanogaster egg-laying site selection offers a genetic model to study a simple form of value-based decision. We have previously shown that Drosophila females consistently reject a sucrose-containing substrate and choose a plain (sucrose-free) substrate for egg laying in our sucrose versus plain decision assay. However, either substrate is accepted when it is the sole option. Here we describe the neural mechanism that underlies females' sucrose rejection in our sucrose versus plain assay. First, we demonstrate that females explored the sucrose substrate frequently before most egg-laying events, suggesting that they actively suppress laying eggs on the sucrose substrate as opposed to avoiding visits to it. Second, we show that activating a specific subset of DA neurons triggered a preference for laying eggs on the sucrose substrate over the plain one, suggesting that activating these DA neurons can increase the value of the sucrose substrate for egg laying. Third, we demonstrate that neither ablating nor inhibiting the mushroom body (MB), a known Drosophila learning and decision center, affected females' egg-laying preferences in our sucrose versus plain assay, suggesting that MB does not mediate this specific decision-making task. We propose that the value of a sucrose substrate- as an egg-laying option-can be adjusted by the activities of a specific DA circuit. Once the sucrose substrate is determined to be the lesser valued option, females execute their decision to reject this inferior substrate not by stopping their visits to it, but by actively suppressing their egg-laying motor program during their visits. Copyright © 2015 the authors 0270-6474/15/351396-15$15.00/0.


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