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

Abstract

Selection of appropriate oviposition sites is essential for progeny survival and fitness in generalist insect species, such as Drosphila 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 eggdeposition. 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.choice behavior ͉ gustatory system ͉ olfactory system ͉ mushroom body ͉ ellipsoid body O viposition provides a powerful yet simple means for monitoring preference behavior in Drosophila melanogaster, since a laid egg represents a marker for female position. Past studies have used egg laying as a readout for conditions advantageous to progeny development (1, 2), in which oviposition preference effectively separates larvae of different sibling species of Drosophila. Egg laying has also been used to detect aversion toward compounds toxic to both larvae and adults (3, 4). Furthermore, numerous studies have used patterns of oviposition to distinguish subtle differences in host plant preferences, which have provided insights into resource requirements and ecological behaviors of different Drosophila species (5, 6).Despite numerous studies using oviposition-site selection as a behavioral readout, direct study of the relevant sensory circuits and the oviposition program itself have been initiated only recently in D. melanogaster (7,8). To investigate the genetic mechanisms and neural circuits regulating this important behavioral choice in D. melanogaster, we developed a simple yet robust 2-choice assay that utilizes acetic acid (AA), a naturally occurring product of fruit fermentation, as an egg-laying attractant (9, 10). However, in addition to verifying a strong egg-laying preference for AA, we surprisingly observed D. melanogaster show a strong positional aversion to the same AA-containing food. We demonstrate that when sampling for oviposition sites, females integrate input from distinct sensory modalities to choose a particular behavioral output from 2 competing options: ovipositional attraction for and positional repulsion to AA. Egg-laying preference is p...

Flying the Fly: Long-range Flight Behavior of Drosophila melanogaster to Attractive Odors

“…Sensitivity to acetic acid is expressed in D. melanogaster adults and larvae (Hoffmann and Parsons 1984;Cobb 1999;Ruebenbauer et al 2008;Joseph et al 2009), supporting the idea that this compound is of ecological relevance. Acetic acid probably serves as a cue for the presence of fermenting fruit and other substrates used as food or oviposition sites.…”

“…Interestingly, Joseph et al (2009) (Table 2). It will be rewarding to study the representation of defined blends of synthetic compounds in comparison with complex authentic odors such as vinegar.…”

Agar-polydimethylsiloxane devices for quantitative investigation of oviposition behaviour of adult Drosophila melanogaster

“…1), and the oviposition and viability of flies (25 females and 20 males) were quantitatively investigated. When compared to conventional oviposition assays, our technique has provided a Surface quality, texture, and chemistry have been shown to have significant effects on flies' oviposition, 24,25,30,31,[33][34][35][36][37] however, the required area of exposure to agar substrate, in order to keep a population of fruit flies alive and to induce them to lay their eggs naturally (i.e., similarly to pure agar substrates) were not investigated. Accordingly, our aim was to quantitatively investigate the effects and the threshold values of surface exposure area on oviposition of fruit flies using our PDMS membrane patterning technique.…”

“…Other studies have likewise shown ovipositional preferences towards chemicals such acetic acid and limonene but avoidance from harmful ones like geosmin. 24,36,37 These techniques and studies have greatly enhanced our overall understanding of oviposition behaviour. However, they lack the accuracy, sensitivity and control, as well as the adequate level of repeatability that is required for parametric and quantitative investigation of viability and oviposition of fruit flies on agar substrates, especially in response to precise variations in surface exposure area and physical size of the oviposition site as well as the chemical and mechanical properties of the agar substrate.…”

“…[15][16][17][18][19] Therefore, oviposition is used as a metric quantity to provide a clear indication of flies' sensory system health and their overall fitness (the ability to survive and reproduce). 24,25 It is used predominately in developmental, 26 chemical screening, 27 and toxicology 28,29 studies as a simple and effective readout indicator. It is also of interest to biologists for answering fundamental questions about oviposition and reproduction patterns in insects.…”