Sexually dimorphic effects of dietary sugar on lifespan, feeding and starvation resistance in Drosophila

Abstract

Lifespan and health in older age are strongly influenced by diet. Feeding Drosophila melanogaster diets high in sugar has increasingly been used as an experimental model to understand the physiological effects of unhealthy, contemporary human diets. Several metabolic parameters and physiological responses to nutrition are known to be dependent on the sex of the animal. However, sexual dimorphism in the responses to high-sugar diets in fruit flies has not been examined. Here we show that a high-sugar diet in Drosophila melanogaster elicits sexually dimorphic effects on feeding behaviour, starvation resistance and lifespan. Females feed less on such diets, while males feed more, and these feeding responses may have secondary consequences. Females, more than males, gain the ability to resist periods of starvation from high-sugar diets, indicating that the female response to excess sugar may be geared towards surviving food shortages in early life. At the same time, female lifespan is more susceptible to the detrimental effects of high sugar diets. Our study reveals differences between Drosophila sexes in their responses to sugar-rich diets, indicating the fruit fly could be used as a model to understand the sexually dimorphic features of human metabolic health.

Sexual dimorphism in the nutritional requirement for adult lifespan in Drosophila melanogaster

“…Drosophila melanogaster has been used as a model for nutritional physiology studies for many years (Piper, 2017;Rauser, Mueller, & Rose, 2004;Tatar, Post, & Yu, 2014), and their requirements for development and female reproduction are well studied (Begg & Robertson, 1950;Consuegra et al, 2019;Piper, 2017;Sang & King, 1961). We also know that the lifespan of male and female adults respond differently to dietary interventions and that the sexes show different preference in macronutrient balance (Bowman & Tatar, 2016;Camus, Huang, Reuter, & Fowler, 2018;Chandegra, Tang, Chi, & Alic, 2017;Lee, Kim, & Min, 2013;Magwere, Chapman, & Partridge, 2004;Regan et al, 2016;Wu et al, 2020), but no one has systematically determined the minimal requirements of each nutrient class for adult lifespan and whether these requirements differ between the sexes. Defining these limits is important since it is fundamental to understanding how adult-specific diet interventions, such as DR and DB, may be operating to modify lifespan.…”

Gene-diet interactions: dietary rescue of metabolic defects inspen-depleted Drosophila

“…rescues Spen-KD adult lifespans. Unlike the high-protein diet, excess carbohydrates is 564 beneficial and confers starvation resistance in mated females, and to a lesser extent 565 males (Chandegra et al 2017). As described in our previous study, Spen-KD alters 566 carbohydrate metabolism and changes glycolytic flux (Hazegh et al 2017).…”

“…We see in 567 the adult stage wherein HSD is a more favorable diet composition for longevity of Spen-568 KD mated females than do CTRL-KD. This is not conserved in males, which is not 569 entirely surprising given the significantly smaller benefit of increased sugar conferred to 570 adult males in general (Chandegra et al 2017). HSD alters the metabolite profiles of 571…”

A subset of brain neurons controls regurgitation in adult Drosophila melanogaster

“…Although we found no sexual dimorphism in the pattern of VT041723-GAL4 expression in the brain (data not shown), a closer look at the expression of sex-specific fru and dsx in VT041723-GAL4 neurons would provide further insight into possible mechanisms underlying sexual dimorphism. In addition, sexspecific differences in feeding responses to salt (Walker et al, 2015), yeast (Ribeiro and Dickson, 2010), amino acids (Ganguly et al, 2017) and sugars (Chandegra et al, 2017) have been reported. Given the possibility of functional connectivity between VT041723-GAL4 neurons and peripheral taste neurons, it will be of interest to determine whether specific gustatory input is involved in sexdependent variation in the proboscis holding phenotype.…”