PT - JOURNAL ARTICLE AU - Elisa Dell’Aglio AU - Virginie Lacotte AU - Sergio Peignier AU - Isabelle Rahioui AU - Fadéla Benzaoui AU - Agnès Vallier AU - Pedro Da Silva AU - Emmanuel Desouhant AU - Abdelaziz Heddi AU - Rita Rebollo TI - Diet as a major driver of endosymbiont proliferation in cereal weevils AID - 10.1101/2022.07.06.498660 DP - 2022 Jan 01 TA - bioRxiv PG - 2022.07.06.498660 4099 - http://biorxiv.org/content/early/2022/07/06/2022.07.06.498660.short 4100 - http://biorxiv.org/content/early/2022/07/06/2022.07.06.498660.full AB - Nutritional symbiosis between insects and intracellular bacteria (endosymbionts) are a major force of adaptation, allowing animals to colonize nutrient-poor ecological niches1–6. Many beetles feeding on tyrosine-poor substrates rely on a surplus of aromatic amino acids produced by bacterial endosymbionts7–9 that synthesize them autotrophically10–13. This surplus of aromatic amino acids is crucial for the biosynthesis of a thick exoskeleton, the cuticle, which is made of a matrix of chitin with proteins and pigments built from the tyrosine-derived 3,4-dihydroxyphenylalanine (DOPA14), providing an important defensive barrier against biotic and abiotic stress10,15. Other endosymbiont-related advantages for beetles include a faster development4,16 and improved fecundity17,18. The association between the cereal weevil Sitophilus oryzae and Sodalis pierantonius endosymbiont19 represents a unique case study: in young adult weevils, endosymbionts undergo a massive proliferation concomitant with the cuticle tanning, then they are fully eliminated20. While endosymbiont clearance is a host-controlled process20, the mechanism triggering endosymbiont proliferation remains poorly understood. Here, we show that endosymbiont proliferation relies on host carbohydrate intake. Remarkably, insect fecundity was preserved, and the cuticle tanning achieved, even when endosymbiont proliferation was experimentally blocked, except in the context of a severely unbalanced diet. Moreover, a high endosymbiont load coupled with nutrient shortage dramatically impacts host survival, revealing the high energy cost of proliferating endosymbionts and the incapacity of the host to adjust energy allocation.Highlightsin the cereal weevil Sitophilus oryzae, carbohydrate intake triggers an exponential endosymbiont proliferation in young adults, before a host-controlled endosymbiont clearance;the host is incapable of adjusting energy allocation to the endosymbionts, even to the detriment of its own survival;on a balanced diet, endosymbiont proliferation is dispensable for host fitness (cuticle tanning and fecundity).Competing Interest StatementThe authors have declared no competing interest.