Adult fruit fly attraction to larvae biases experience and mediates social learning

Durisko, Zachary; Anderson, Blake; Dukas, Reuven

doi:10.1242/jeb.097683

Cited by 27 publications

(21 citation statements)

References 42 publications

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“…Furthermore, larvae and adults learn to prefer odours from food substrates that have been occupied by larvae over odours from unoccupied substrates of similar quality (Durisko and Dukas, 2013;Durisko et al, 2014). Our controlled experiments indicated that the social attraction we documented was not caused by odours from either fruit or yeast.…”

Section: Introductionmentioning

confidence: 53%

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Social attraction mediated by fruit flies' microbiome

Venu

Durisko

et al. 2014

Journal of Experimental Biology

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107

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Larval and adult fruit flies are attracted to volatiles emanating from food substrates that have been occupied by larvae. We tested whether such volatiles are emitted by the larval gut bacteria by conducting tests under bacteria-free (axenic) conditions. We also tested attraction to two bacteria species, Lactobacillus brevis, which we cultured from larvae in our lab, and L. plantarum, a common constituent of fruit flies' microbiome in other laboratory populations and in wild fruit flies. Neither larvae nor adults showed attraction to axenic food that had been occupied by axenic larvae, but both showed the previously reported attraction to standard food that had been occupied by larvae with an intact microbiome. Larvae also showed significant attraction to volatiles from axenic food and larvae to which we added only either L. brevis or L. plantarum, and volatiles from L. brevis reared on its optimal growth medium. Controlled learning experiments indicated that larvae experienced with both standard and axenic used food do not perceive either as superior, while focal larvae experienced with simulated used food, which contains burrows, perceive it as superior to unused food. Our results suggest that flies rely on microbiome-derived volatiles for longdistance attraction to suitable food patches. Under natural settings, fruits often contain harmful fungi and bacteria, and both L. brevis and L. plantarum produce compounds that suppress the growth of some antagonistic fungi and bacteria. The larval microbiome volatiles may therefore lead prospective fruit flies towards substrates with a hospitable microbial environment.

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Section: Introductionmentioning

confidence: 53%

“…larvae in tests with wild-caught larval and adult fruit flies as well as in experiments using natural fruit (Durisko and Dukas, 2013;Durisko et al, 2014). Volatiles from both L. brevis, which we cultured from our fly population, and L. plantarum, which has been isolated from the Drosophila gut in other studies, were attractive.…”

Section: P=01mentioning

confidence: 99%

Social attraction mediated by fruit flies' microbiome

Venu

Durisko

et al. 2014

Journal of Experimental Biology

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107

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“…We used a protocol modified from Durisko et al [30]. We placed each recently mated female inside a plastic cage (15 cm wide, 30 cm long, and 15 cm high), which contained two 35 mm Petri dishes placed at the opposite far corners of each cage.…”

Section: Methodsmentioning

confidence: 99%

The Value of Patch-Choice Copying in Fruit Flies

Golden

Dukas

2014

PLoS ONE

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Many animals copy the choices of others but the functional and mechanistic explanations for copying are still not fully resolved. We relied on novel behavioral protocols to quantify the value of patch-choice copying in fruit flies. In a titration experiment, we quantified how much nutritional value females were willing to trade for laying eggs on patches already occupied by larvae (social patches). Females were highly sensitive to nutritional quality, which was positively associated with their offspring success. Females, however, perceived social, low-nutrition patches (33% of the nutrients) as equally valuable as non-social, high-nutrition ones (100% of the nutrients). In follow-up experiments, we could not, however, either find informational benefits from copying others or detect what females' offspring may gain from developing with older larvae. Because patch-choice copying in fruit flies is a robust phenomenon in spite of potential costs due to competition, we suggest that it is beneficial in natural settings, where fruit flies encounter complex dynamics of microbial communities, which include, in addition to the preferred yeast species they feed on, numerous harmful fungi and bacteria. We suggest that microbial ecology underlies many cases of copying in nature.

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“…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). These results suggest that Drosophila adults may rely on microbe-derived volatiles for long-distance attraction to suitable feeding and egg-laying sites.…”

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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Adult fruit fly attraction to larvae biases experience and mediates social learning

Cited by 27 publications

References 42 publications

Social attraction mediated by fruit flies' microbiome

Social attraction mediated by fruit flies' microbiome

The Value of Patch-Choice Copying in Fruit Flies

Gut microbiota affects development and olfactory behavior in Drosophila melanogaster

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