Highlights d Intestinal carbohydrate metabolism is male-biased and region-specific d Testes masculinize gut sugar handling by promoting enterocyte JAK-STAT signaling d The male intestine secretes citrate to the adjacent testes d Gut-derived citrate promotes food intake and sperm

Reproduction induces increased food intake across females of many animal species 1 – 4 , providing a physiologically relevant paradigm for exploration of appetite regulation. Parsing enteric neuronal diversity in Drosophila , we identify a key role for gut-innervating neurons with sex- and reproductive state-specific activity in sustaining the increased food intake of mothers during reproduction. Steroid and enteroendocrine hormones functionally remodel these neurons, leading to post-mating release of their neuropeptide onto the muscles of the crop: a stomach-like organ. Post-mating neuropeptide release changes the dynamics of crop enlargement, resulting in increased food intake. Preventing enteric neuron remodelling blunts reproductive hyperphagia and reduces reproductive fitness. Thus, plasticity of enteric neurons is key to reproductive success. Our findings provide a new mechanism to attain the positive energy balance that sustains gestation which, if dysregulated, could contribute to infertility or weight gain.

The eggshell serves as a depository for proteins that play an important role in early embryonic development. In particular, the Drosophila eggshell is responsible for transferring asymmetries from the egg chamber to specify the regions at both ends of the embryo through the uneven activation of the Torso (Tor) receptor in its membrane. This process relies on the restricted expression of the gene torso-like (tsl) in subpopulations of follicle cells during oogenesis and its protein accumulation at both poles of the eggshell, but it is not known how this signal is transmitted to the embryo. Here, we show that Tsl accumulates at the embryonic plasma membrane, even in the absence of the Tor receptor. However, during oogenesis, we detected Tsl accumulation only at the eggshell. These results suggest that there is a two-step mechanism to transfer the asymmetric positional cues from the egg chamber into the early embryo: initial anchoring of Tsl at the eggshell as it is secreted, followed by its later translocation to the egg plasma membrane, where it enables Tor receptor activation. Translocation of anchored determinants from the eggshell might then regulate the spatial and temporal control of early embryonic developmental processes.