Adaptation to Chronic Nutritional Stress Leads to Reduced Dependence on Microbiota in Drosophila melanogaster

Abstract

Numerous studies have shown that animal nutrition is tightly linked to gut microbiota, especially under nutritional stress. In Drosophila melanogaster, microbiota are known to promote juvenile growth, development, and survival on poor diets, mainly through enhanced digestion leading to changes in hormonal signaling. Here, we show that this reliance on microbiota is greatly reduced in replicated Drosophila populations that became genetically adapted to a poor larval diet in the course of over 170 generations of experimental evolution. Protein and polysaccharide digestion in these poor-diet-adapted populations became much less dependent on colonization with microbiota. This was accompanied by changes in expression levels of dFOXO transcription factor, a key regulator of cell growth and survival, and many of its targets. These evolutionary changes in the expression of dFOXO targets to a large degree mimic the response of the same genes to microbiota, suggesting that the evolutionary adaptation to poor diet acted on mechanisms that normally mediate the response to microbiota. Our study suggests that some metazoans have retained the evolutionary potential to adapt their physiology such that association with microbiota may become optional rather than essential.

Host diet mediates a negative relationship between abundance and diversity ofDrosophilagut microbiota

“…in 4% and 10% diets becomes notably low on 27%. However, our results imply that microbiota abundance declines exponentially with dietary yeast content; yet it is on diets with low yeast content that microbiota become crucial to maintain healthy growth and survival of the Drosophila host (Erkosar et al., , ; Ridley, Wong, Westmiller, & Douglas, ; Shin et al., ; Storelli et al., ). Thus, the microbiota become scarce under the dietary conditions in which the host particularly needs them.…”

“…Shifts in microbiota composition are correlated with changes in host metabolism in mammals (Goodrich et al, 2014), and growthpromoting effects have been attributed to specific members of the Drosophila microbiota (Erkosar, Kolly, Van Der Meer, & Kawecki, 2017;Shin et al, 2011;Storelli et al, 2011). However, whether microbiota diversity in itself affects host fitness remains unclear, although gut microbiota diversity was found to be positively correlated with human metabolic health (Le Chatelier et al, 2013).…”

Comparison of gut bacterial communities and their associations with host diets in four fruit borers

“…The gut bacterial diversity of termites and cockroaches revealed that host phylogeny was an important factor that determined gut microbial composition . Additionally, the abundance and structure of microbiota in Drosophila suzukii were strongly affected by the nutritional situation . Studies of ground‐dwelling beetles and cabbage white butterfly showed that the microbial composition was dominated by common environmental taxa .…”

“…Recently, a growing number of studies have cataloged and characterized microbial communities, particularly in bees, fruit flies, termites, and beetles . For example, a simple and distinctive gut microbiota, consisting of eight bacterial phylotypes, has been found in honey bees .…”

Sexual selection reveals a cost of pathogen resistance undetected in life‐history assays

“…; Erkosar et al. ). None of these hypothetical mechanisms would explain why costs of resistance should be expressed in traits affecting male success and not in life‐history traits.…”