C. elegans sperm and oocytes differentially transmit diet-induced adaptations to their progeny

Non-genetic inheritance allows organisms to transmit recently acquired adaptive information to progeny to maximize fitness in response to environmental change. While Caenorhabditis elegans exhibits persistent multigenerational responses to transient stress, how non-genetic mechanisms respond to multigenerational environmental change remains largely unexplored. As a bacterivore exposed to diverse microbes, C. elegans offers a powerful model to study adaptation to a persistent environmental change. We measured reproductive fitness via hermaphrodite self-brood size and found that novel diets often caused 20-45% brood-size reductions compared to controls. However, animals adapt to the new diet producing normal-sized broods within 5 to 10 generations. However, these adapted animals often became maladapted to their previous diet but could re-adapt within a similar timeframe. This rapidity and reversibility, which was also observed in genetically identical isogenic lines, strongly suggest a non-genetic mechanism. Phenotypic analyses of maladapted animals revealed a correlation between specific diets and germline defects primarily affecting either sperm or oocytes. Crosses between differently adapted parents demonstrated that sperm primarily transmitted sperm adaptations and oocytes primarily transmitted oocyte adaptations. Together, these results highlight the critical role of non-genetic inheritance as a flexible and heritable mechanism enabling organisms to rapidly adapt to unpredictable environmental change.