Sexual Dimorphism in Metabolic Responses to Western Diet in Drosophila melanogaster

Abstract

Obesity is a chronic disease affecting millions of people worldwide. The fruit fly (Drosophila melanogaster) is an interesting research model to study metabolic and transcriptomic responses to obesogenic diets. However, the sex-specific differences in these responses are still understudied and perhaps underestimated. In this study, we exposed adult male and female Dahomey fruit flies to a standard diet supplemented with sugar, fat, or a combination of both. The exposure to a diet supplemented with 10% sugar and 10% fat efficiently induced an increase in the lipid content in flies, a hallmark for obesity. This increase in the lipid content was more prominent in males, while females displayed significant changes in the glycogen content. The strong effects of the diets on the ovarian size and number of mature oocytes were also present in females exposed to diets supplemented with fat and a combination of fat and sugar. In both males and females, the fat body morphology changed and was associated with an increase in the lipid content of fat cells in response to the diets. The expression of metabolism-related genes also displayed a strong sexually dimorphic response under normal conditions and in response to the sugar and/or fat-supplemented diets. Here, we showed that the exposure of adult fruit flies to an obesogenic diet containing both sugar and fat allowed studying sexual dimorphism in metabolism and the expression of genes regulating metabolism.

Drosophila melanogaster as a Model Organism for Obesity and Type-2 Diabetes Mellitus by Applying High-Sugar and High-Fat Diets

“…Interestingly, male flies exposed to HSD for 30 days did not show an accumulation of either glucose or TAG, nor a reduction in the climbing ability, suggesting that aging in male D. melanogaster may result in flies being more resistant to metabolic changes [ 36 ]. Sex-dependent responses in TAG accumulation have been described previously, confirming that females develop larger fat cells than males on western diets supplemented with sugar and fat (10–20%) [ 18 ], suggesting a key role in successful reproduction [ 37 ].…”

“…In the present study, both dietary modifications produced decreases in lifespan, while the effect was more pronounced in females than in males, with the latter only being affected by HSD from 20 days of treatment. Sex differences in response to nutritional variations have been recently and widely reported in D. melanogaster [ 18 , 19 , 20 , 21 ], as well as in a range of species; however, the genetic and molecular bases for this dimorphism are often unknown. Previous investigations point to (a) differences in reproductive gene responses mediated by the classical nutrient-sensing pathway IIS/TOR [ 22 ] and (b) sexual dimorphism in the intestinal tract [ 23 ] as the main factors influencing the adaptive responses of D. melanogaster to the dietary environment.…”

“…Previous investigations point to (a) differences in reproductive gene responses mediated by the classical nutrient-sensing pathway IIS/TOR [ 22 ] and (b) sexual dimorphism in the intestinal tract [ 23 ] as the main factors influencing the adaptive responses of D. melanogaster to the dietary environment. Accordingly, recent studies revealed mated females as more sensitive than males to HSD and HFD, suggesting higher intestinal stem cell proliferation in mated females as a responsible factor in reducing the lifespan and increasing nutrient absorption [ 18 , 19 , 23 , 24 , 25 ]. Undoubtedly, adaptation to reproductive functions is the main cause of sex differences, as carbohydrates are the source of energy that males need for mating, while females mainly invest in proteins for providing eggs [ 21 , 26 ].…”

“…In our work, the sum of those diet effects may explain why fly weights did not change over the 30 days of the experiment. For instance, mating may have influenced the weight in females, as it has been described that diets supplemented with fat and/or sugar affect oogenesis, a decrease in the size of the ovaries and, consequently, weight [ 18 ]. However, the increased lipid and/or carbohydrate accumulation caused by increased insulin signaling would counteract this effect [ 29 ].…”

Drosophila suzukii energetic pathways are differently modulated by nutritional geometry in males and females

“…The outcome is however different when using fruit media, with flies having a higher preference and better energetic fitness in fruit-based media containing higher P:C 25 , 26 . Additionally, the influence of sex, previously highlighted for D. melanogaster 7 , 27 , remains unexplored for SWD. With such variable results related to preference and oviposition site selection, understanding how different hosts may influence SWD adults (and their progenies) in terms of metabolic fitness and energetic signaling pathways could give a better insight into the behavior and biology of this species, as is being proposed for D. melanogaster 28 , 29 .…”