Extreme longevity of highly fecund termite queens achieved by mitochondrial and insulin upregulation without harmful lipid signatures or accumulation

Eusocial termite queens achieve nearly maximal fertility throughout their extremely long life without apparent signs of aging. Termites represent, therefore, an ideal model for aging research. To investigate the molecular mechanisms underlying their long reproductive life, we carried out transcriptomic, lipidomic and metabolomic analyses on fat bodies of sterile short lived workers, long-lived kings and five stages spanning twenty years of adult queen maturation. In mature reproductives, genes supporting a robust mitochondrial functioning or associated with genome stability were upregulated. In most organisms, insulin signaling increases fertility but decreases lifespan, often accompanied by harmful lipid signatures. Our findings suggest that an upregulation of insulin-like peptide (Ilp9) in the fat body of termite queens is accompanied by a specific lipid metabolism, limiting fat storage, thus sustaining both high fertility and maintaining extreme lifespan. Our results highlight potential molecular targets for research into aging-related metabolic diseases linked to the accumulation of excess fat.