The Transcriptome in Transition: Global Gene Expression Profiles of Young Adult Fruit Flies Depend More Strongly on Developmental Than Adult Diet

Developmental diet is known to exert long-term effects on adult phenotypes in many animal species as well as disease risk in humans, purportedly mediated through long-term changes in gene expression. However, there are few studies linking developmental diet to adult gene expression. Here, we use a full-factorial design to address how three different larval and adult diets interact to affect gene expression in 1-day-old adult fruit flies (Drosophila melanogaster) of both sexes. We found that the largest contributor to transcriptional variation in young adult flies is larval, and not adult diet, particularly in females. We further characterized gene expression variation by applying weighted gene correlation network analysis (WGCNA) to identify modules of co-expressed genes. In adult female flies, the caloric content of the larval diet associated with two strongly negatively correlated modules, one of which was highly enriched for reproduction-related processes. This suggests that gene expression in young adult female flies is in large part related to investment into reproduction-related processes, and that the level of expression is affected by dietary conditions during development. In males, most modules had expression patterns independent of developmental or adult diet. However, the modules that did correlate with larval and/or adult dietary regimes related primarily to nutrient sensing and metabolic functions, and contained genes highly expressed in the gut and fat body. The gut and fat body are among the most important nutrient sensing tissues, and are also the only tissues known to avoid histolysis during pupation. This suggests that correlations between larval diet and gene expression in male flies may be mediated by the carry-over of these tissues into young adulthood. Our results show that developmental diet can have profound effects on gene expression in early life and warrant future research into how they correlate with actual fitness related traits in early adulthood.