Direct and trans-generational effects of male and female gut microbiota in Drosophila melanogaster

Abstract

There is increasing evidence of the far-reaching effects of gut bacteria on physiological and behavioural traits, yet the fitness-related consequences of changes in the gut bacteria composition of sexually interacting individuals remain unknown. To address this question, we manipulated the gut microbiota of fruit flies, Drosophila melanogaster, by monoinfecting flies with either Acetobacter pomorum (AP) or Lactobacillus plantarum (LP). Re-inoculated individuals were paired in all treatment combinations. LP-infected males had longer mating duration and induced higher short-term offspring production in females compared with AP-infected males. Furthermore, females of either re-inoculation state mated with AP-infected males were more likely to have zero offspring after mating, suggesting a negative effect of AP on male fertility. Finally, we found that the effects of male and female gut bacteria interacted to modulate their daughters', but not sons' body mass, revealing a new trans-generational effect of parental gut microbiota. In conclusion, this study shows direct and trans-generational effects of the gut microbiota on mating and reproduction.

Microbiome‐Germline Interactions and Their Transgenerational Implications

“…Removal of gut microbiota in one generation therefore unmasked a genetic impact in the following generation. A more recent study provided additional evidence for transgenerational impacts of gut bacteria, indicated by differences between parent and offspring . Specifically, it found that mating of LP‐(mono)‐associated males with either LP‐ or AP‐(mono)‐associated females produced daughters with higher body mass compared to daughters of AP‐associated males.…”

“…Additional evidence for modulation of reproductive functions extracellular gut bacteria has recently been provided in Drosophila by analyzing outcomes of mating between flies that were mono‐associated with either Acetobacter pomorum (AP) or Lactobacillus plantarum (LP) . Mating duration and number of offspring produced over a 72 hr period were both higher for crosses with LP‐associated males compared to AP‐associated males.…”

Health and environmental applications of gut microbiome: a review

“…Similar kind of study on Drosophila melanogaster was published by Sharon et al [63] using molasses and starch as rearing media, where the mating preference of these flies appeared only after one generation and was maintained for at least 37 generations. Interestingly, mating preference was abolished after a treatment with antibiotic, signifying the important role of microbiota of fly gut for the phenomenon [64]. These observations triggered the scientific community to study further on the speciation and evolution of a population based on dietary substances.…”

“…It has already been known that mating preferences in flies depend upon several factors like environmental conditions, such as humidity, temperature, pH of the rearing media, diet etc. [64,[67][68][69]. Dodd [68] primarily reported the positive assortative mating in Drosophila pseudoobscura that preferred mating partners reared for more than 25 generations in the same media: the flies reared on either starch-based or maltose-based media preferred mating partner came out from their own rearing media developing a population either of "starch flies" or "maltose flies".…”

“…One of the important mechanisms for the origin of new species is mating preference through the selection of partner [63,64]. The concept of speciation rests on the origin of isolating barriers that prevent actual or potential gene flow among populations and thereafter identification of the traits along with the evolutionary forces that control these traits [65,66].…”