Sex-Dependent Effects of the Microbiome on Foraging and Locomotion in Drosophila suzukii

Abstract

There is growing evidence that symbiotic microbes can influence multiple nutrition-related behaviors of their hosts, including locomotion, feeding, and foraging. However, how the microbiome affects nutrition-related behavior is largely unknown. Here, we demonstrate clear sexual dimorphism in how the microbiome affects foraging behavior of a frugivorous fruit fly, Drosophila suzukii. Female flies deprived of their microbiome (axenic) were consistently less active in foraging on fruits than their conventional counterparts, even though they were more susceptible to starvation and starvation-induced locomotion was notably more elevated in axenic than conventional females. Such behavioral change was not observed in male flies. The lag of axenic female flies but not male flies to forage on fruits is associated with lower oviposition by axenic flies, and mirrored by reduced food seeking observed in virgin females when compared to mated, gravid females. In contrast to foraging intensity being highly dependent on the microbiome, conventional and axenic flies of both sexes showed relatively consistent and similar fruit preferences in foraging and oviposition, with raspberries being preferred among the fruits tested. Collectively, this work highlights a clear sex-specific effect of the microbiome on foraging and locomotion behaviors in flies, an important first step toward identifying specific mechanisms that may drive the modulation of insect behavior by interactions between the host, the microbiome, and food.

Nutritional phenotype underlines the performance trade-offs of Drosophila suzukii on different fruit diets

“…Previously, our work has established that when given different fruit choices, female D. suzukii tended to forage and oviposit on the raspberries over strawberries, blueberries, nectarines, and grapes ( Shu et al., 2021 ). The relative fruit preferences were largely unaffected by the flies’ microbiome, developmental and transgenerational diet histories, signifying a robust innate behavior.…”

“…In our recent study using five different host fruits (raspberries, strawberries, blueberries, nectarines, and grapes), we have established that D. suzukii has clear fruit preferences in foraging and oviposition and that these preferences were not influenced by the fly's developmental diet history or gut microbiome ( Shu et al., 2021 ). In addition to varied attractiveness to D. suzukii , these fruits differ widely in nutrient content, with protein-to-sugar ratio (P:S) ranging from 1:4 (raspberries) to 1:22 (grapes).…”

Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive pest fly

“…Second, the yeasts and bacteria in fruits represent an important source of protein for the egg-to-adult survival of D. suzukii (Lewis & Hamby, 2019; Bing et al, 2021). Moreover, the presence of microbes has been shown to modify the foraging behavior of D. suzukii females (Shu et al, 2021a), their oviposition preference and offspring performance (Bellutti et al, 2018). Therefore, if the microbial community differs among cherry, strawberry and blackberry, our results could be at least partly explained by the nutritional effect of a fly microbiome transmitted over generations rather than to a genetic effect.…”

“…Second, the yeasts and bacteria in fruits represent an important source of protein for the egg-to-adult survival of D. suzukii (Lewis & Hamby, 2019;Bing et al, 2021). Moreover, the presence of microbes has been shown to modify the foraging behavior of D. suzukii females (Shu et al, 2021a), their oviposition preference and offspring performance (Bellutti et al, 2018).…”

Enterobacter sp. AA26 as a Protein Source in the Larval Diet of Drosophila suzukii

“…Interestingly, Enterobacter sp. has been identified in few D. suzukii studies with varying diversity and abundance [52,53,57].…”