Disentangling the reproductive and metabolic transcriptional responses to diet in Drosophila melanogaster

Nutrition significantly influences various life-history traits in organisms, impacting decisions about growth, reproduction, and longevity. Accordingly, previous studies in Drosophila have demonstrated that diet affects transcription regulation, with many genes exhibiting altered expression, for example, between protein- and carbohydrate-rich diets. It remains challenging, however, to distinguish between metabolic adaptations to the different diets themselves and regulation pertaining to life-history responses to nutrient availability. In this study, we explore the transcriptomic responses of virgin and mated flies to changes in nutritional environments, with the aim to differentiate changes in metabolism from changes due to altered reproductive investment. Using RNA-seq, we show that while males only respond to diet, both nutritional conditions and mating status affect gene expression in females. By comparing responses between males and females and virgin and mated flies, we are able to differentiate between basal dietary responses and reproductive adaptations, with the latter involving 8 times as many genes as the former. We identify GATA family transcription factors and the heat shock factor (Hsf) as crucial regulators of diet-dependent reproductive genes. These findings enhance our understanding of the complex interactions between nutrition and reproductive strategies in Drosophila.