Social attraction mediated by fruit flies' microbiome

Abstract

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.

Drosophila females trade off good nutrition with high quality oviposition sites when choosing foods

“…In nature, nutritional decisions can be complicated by several additional factors such as social information provided by other females (Battesti et al, 2012;Durisko et al, 2014;Lihoreau et al, 2016;Sarin and Dukas, 2009;Chabaud et al, 2009), competition (Eggert et al, 2008;Salomon et al, 2008), sexual interactions with males (Chapman and Partridge, 1996;Gorter et al, 2016) or the presence of beneficial microbial communities on foods (Venu et al, 2014;Wong et al, 2015). Thanks to their unique association with food as shelter, breeding sites and sources of nutrients, fruit flies hold considerable promise as model organisms with which to study these multi-level nutritional interactions within the extended integrative framework of nutritional ecology (Simpson et al, 2015a).…”

Collective selection of food patches in Drosophila

“…Previous studies point towards a role of long-distance chemical communication leading to aggregation (Dubnau, 2014;Sokolowski, 2010). For instance, feeding larvae are attracted to each others by odors derived from the gut bacteria of conspecifics as well as by physical heterogeneities generated on the substrate surface as a result of their digging activities (Durisko and Dukas, 2013;Venu et al, 2014). Adults respond to a volatile sex pheromone (cVA) produced by males and transferred to females during copulation (Bartelt et al, 1985;Butterworth, 1969;Wertheim et al, 2005).…”

Social structure and indirect genetic effects: genetics of social behaviour

“…Socially responsive flies preferentially aggregate on sites that have been socially vetted and whose genetic composition is suitable, as decisions are based on behavioural and chemical cues within the aggregate (Saltz, 2011;Simon et al, 2012;Venu et al, 2014). D. melanogaster interact between and among themselves in patterns that are at least in part genetically determined (Schneider et al, 2012) and that shape the interactive social environment within the larger group.…”