Nutritional stress in larvae induces adaptive responses that transcend generations in males of a model insect

The ability of organisms to cope with poor quality nutrition is essential for their persistence. For species with a short generation time, the nutritional environments can transcend generations, making it beneficial for adults to prime their offspring to particular diets. However, our understanding of adaptive generational responses, including those to diet quality, are still very limited. Here, we used the vinegar fly, Drosophila melanogaster, to investigate whether females developing as larvae on a nutritionally poor diet produce offspring that are primed for nutrient deficiencies in the following generations. We found that females developed on low-quality diets produced offspring that, on similarly low-quality diets, had both increased egg-to-adult viability and starvation tolerance compared with offspring of females experiencing a nutrient-rich diet. When testing the persistence of such generational priming, we found that just one generation of high-quality diet is sufficient to erase the signal of priming. A global transcriptomic profile analysis on male offspring suggests that the observed phenotypic priming is not a constitutive transcriptomic adjustment of adults; instead, offspring are probably primed as larvae, enabling them to initiate an adaptive response as adults when exposed to low-quality diets. Our results support that generational priming is an important adaptive mechanism that enables organisms to cope with transient nutritional fluctuations.