Drosophila sperm carry a dietary sterol that increases offspring development

Diet affects male fitness directly and across generations. The current research focus is on dietary proteins and carbohydrates. Dietary lipids (DL), which are incorporated into cell membranes and affect signaling, were neglected or analyzed at pathological high-fat diet amounts. How fitness variation arises among males consuming healthy amounts of DL remains unknown, as do the fitness parameters being affected, including paternal effects. Contrasting mammal- vs. plant-derived DL, we measure mating rate, sperm count, sperm and seminal fluid quality, fertility and offspring growth in Drosophila melanogaster. We show that i) mammal-derived DL increased male fitness in isolation and competition, but without changing sperm numbers. ii) We discovered that lipid microcarriers in the seminal fluid fused with, and directly provided DL to sperm, changing sperm quality. iii) Dietary cholesterol, precursor of the growth hormone ecdysone, was incorporated into sperm, vectored to the zygote and improved offspring development and survival. This duality of Drosophila sperm function - fertilization and provision of growth hormone precursor - is an elegant, adaptive solution to prevent rival males from exploiting paternal provision. Direct offspring benefits vectored by sperm offer additional and alternative explanations for the evolution of sperm competition, sperm gigantism, and of anisogamy, the driver of sexual selection.