Seminal fluid is rich in sugars, but their role beyond supporting sperm motility is unknown. In this study, we found Drosophila melanogaster males transfer a substantial amount of a phospho-galactoside to females during mating, but only half as much when undernourished. This seminal substance, which we named venerose, induces an increase in germline stem cells (GSCs) and promotes sperm storage in females, especially undernourished ones. Venerose enters the hemolymph and directly activates nutrient-sensing Dh44+ neurons in the brain. Food deprivation directs the nutrient-sensing neurons to secrete more of the neuropeptide Dh44 in response to infused venerose. The secreted Dh44 then enhances the local niche signal, stimulating GSC proliferation. It also extends the retention of ejaculate by females, resulting in greater venerose absorption and increased sperm storage. In this study, we uncovered the role of a sugar-like seminal substance produced by males that coordinates reproductive responses to nutritional challenges in females.
© 2024. The Author(s).

Nuptial gift-giving or courtship feeding is prevalent across. In an extreme case, females eat male body parts; in another case, females derive nutrients from males’ seminal fluids1. The nursery web spider, Pisaura mirabilis, females store more sperm from nuptial gift-giving males than those offering no gift with the identical copulation duration2. However, it is not known how females evaluate nuptial gifts and adjust sperm storage. Here, we show that Drosophila melanogaster females hold the ejaculate of starved males for shorter period and store less number of their sperm. A knock-down of the sugar transporter Tret1-1 in neurons that express the neuropeptide diuretic hormone 44 (Dh44-PI) critical for the ejaculate holding3 and detection of the nutritional value of sugar4 impairs the female’s ability to adjust the ejaculate holding period according to the male energy status. A galactoside selectively present in the male ejaculate activates Dh44-PI neurons in the brain to secrete Dh44, and starvation reduces its production by approximately 50%. RNAi-knockdown of glycosyltransferases, including UGT305A1, allows males to produce significantly lower amounts of the galactoside without starvation. Females mated with UGT305A1 knockdown males hold the ejaculate shorter, store less sperm and lay fewer eggs. The seminal galactoside enters the female hemocoel during mating, stimulates the activity of Dh44-PI neurons in the brain, augments the secretion of Dh44, and increase the ejaculate holding period, thereby enabling the uptake of injected nutrients and sperm. These evidence suggest that the galactoside signals reflecting the quality of male partners increase sperm storage and may be a source of nutrients used for egg production. Together, this study provides a molecular and cellular framework for understanding how females evaluate courtship feeding and optimize sexual selection after mating.

Recent studies find that sugar tastes less intense to humans with obesity, but whether this sensory change is a cause or a consequence of obesity is unclear. To tackle this question, we study the effects of a high sugar diet on sweet taste sensation and feeding behavior in Drosophila melanogaster. On this diet, fruit flies have lower taste responses to sweet stimuli, overconsume food, and develop obesity. Excess dietary sugar, but not obesity or dietary sweetness alone, caused taste deficits and overeating via the cell-autonomous action of the sugar sensor O-linked N-Acetylglucosamine (O-GlcNAc) transferase (OGT) in the sweet-sensing neurons. Correcting taste deficits by manipulating the excitability of the sweet gustatory neurons or the levels of OGT protected animals from diet-induced obesity. Our work demonstrates that the reshaping of sweet taste sensation by excess dietary sugar drives obesity and highlights the role of glucose metabolism in neural activity and behavior.
Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Animals can determine the nutritional value of sugar without the influence of taste. We examined a Drosophila mutant that is insensitive to the nutritional value of sugars, responding only to the concentration (that is, sweetness). The affected gene encodes a sodium/solute co-transporter-like protein, designated SLC5A11 (or cupcake), which is structurally similar to mammalian sodium/glucose co-transporters that transport sugar across the intestinal and renal lumen. However, SLC5A11 was prominently expressed in 10-13 pairs of R4 neurons of the ellipsoid body in the brain and functioned in these neurons for selecting appropriate foods.