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Kings and queens of eusocial termites can live for decades, while queens sustain a nearly maximal fertility. To investigate the molecular mechanisms underlying their long lifespan, we carried out transcriptomics, lipidomics and metabolomics in Macrotermes natalensis on sterile short-lived workers, long-lived kings and five stages spanning twenty years of adult queen maturation. Reproductives share gene expression differences from workers in agreement with a reduction of several aging-related processes, involving upregulation of DNA damage repair and mitochondrial functions. Anti-oxidant gene expression is downregulated, while peroxidability of membranes in queens decreases. Against expectations, we observed an upregulated gene expression in fat bodies of reproductives of several components of the IIS pathway, including an insulin-like peptide, Ilp9. This pattern does not lead to deleterious fat storage in physogastric queens, while simple sugars dominate in their hemolymph and large amounts of resources are allocated towards oogenesis. Our findings support the notion that all processes causing aging need to be addressed simultaneously in order to prevent it.

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.

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