A nutrient-specific gut hormone arbitrates between courtship and feeding

• Published in: Nature (London) Vol. 602; no. 7898; pp. 632 - 638
• Main Authors: Lin, Hui-Hao, Kuang, Meihua Christina, Hossain, Imran, Xuan, Yinan, Beebe, Laura, Shepherd, Andrew K., Rolandi, Marco, Wang, Jing W.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 24.02.2022; Nature Publishing Group
• Subjects: 14/1; 14/19; 14/35; 14/69; 38/1; 38/35; 38/89; 631/378/1488; 631/378/1804; 631/378/3917; 631/378/3920; 64/24; Amino acids; Animal reproduction; Animals; Arbitration; Behavior; Brain; Calcium imaging; Circuits; Circulatory system; Corazonin protein; Courtship; Diuretics; Drosophila melanogaster - physiology; Drosophila Proteins - metabolism; Feeding; Feeding behavior; Food; Food consumption; Hormones; Humanities and Social Sciences; Insect Hormones - metabolism; Insects; Male; Males; multidisciplinary; Mutation; Neuroimaging; Neurons; Nutrients; Proteins; Science; Science (multidisciplinary); Sexual Behavior, Animal - physiology; Sucrose
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-022-04408-7

Animals must set behavioural priority in a context-dependent manner and switch from one behaviour to another at the appropriate moment 1 – 3 . Here we probe the molecular and neuronal mechanisms that orchestrate the transition from feeding to courtship in Drosophila melanogaster . We find that feeding is prioritized over courtship in starved males, and the consumption of protein-rich food rapidly reverses this order within a few minutes. At the molecular level, a gut-derived, nutrient-specific neuropeptide hormone—Diuretic hormone 31 (Dh31)—propels a switch from feeding to courtship. We further address the underlying kinetics with calcium imaging experiments. Amino acids from food acutely activate Dh31 + enteroendocrine cells in the gut, increasing Dh31 levels in the circulation. In addition, three-photon functional imaging of intact flies shows that optogenetic stimulation of Dh31 + enteroendocrine cells rapidly excites a subset of brain neurons that express Dh31 receptor (Dh31R). Gut-derived Dh31 excites the brain neurons through the circulatory system within a few minutes, in line with the speed of the feeding–courtship behavioural switch. At the circuit level, there are two distinct populations of Dh31R + neurons in the brain, with one population inhibiting feeding through allatostatin-C and the other promoting courtship through corazonin. Together, our findings illustrate a mechanism by which the consumption of protein-rich food triggers the release of a gut hormone, which in turn prioritizes courtship over feeding through two parallel pathways. Diuretic hormone 31 secreted by the gut in response to feeding on protein-rich food excites brain neurons that promote switching from feeding to mating behaviour in Drosophila .