Physiology and metabolism are often sexually dimorphic, but the underlying mechanisms remain
incompletely understood. Here, we use the intestine of Drosophila melanogaster to investigate how
gut-derived signals contribute to sex differences in whole-body physiology. We find that
carbohydrate handling is male-biased in a specific portion of the intestine. In contrast to known
sexual dimorphisms in invertebrates, the sex differences in intestinal carbohydrate metabolism are
extrinsically controlled by the adjacent male gonad, which activates JAK-STAT signalling in
enterocytes within this intestinal portion. Sex reversal experiments establish roles for this malebiased intestinal metabolic state in controlling food intake and sperm production through gutderived citrate. Our work uncovers a male gonad-gut axis coupling diet and sperm production, and
reveals that metabolic communication across organs is physiologically significant. The instructive
role of citrate in inter-organ communication may be significant in more biological contexts than
previously recognised.