Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite

Sarah Séité,Tom J M Van Dooren,Z Wilhelm De Beer,Muriel Andrieu,Arnaud Lemainque,Mark C Harrison,Laure-Anne Poissonnier,José Viscarra,Alain Robert,Mireille Vasseur-Cognet,Hei Sook Sul,Erich Bornberg-Bauer,David Sillam-Dussès,Sébastien Acket,David Renault,Roland Lupoli

doi:10.1038/s42003-021-02974-6

Abstract

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.

Highlights

Kings and queens of eusocial termites can live for decades, while queens sustain a nearly maximal fertility
Specific regions of the gene co-expression network are activated in the fat bodies of different castes and during queen maturation
To study the dramatic adult developmental plasticity shown by M. natalensis termite queens in their reproductive system and fat body during maturation, we carried out a longitudinal study in laboratory colonies established from imagoes collected from the same field colonies (QT0, virgin queens) (“Methods” and Fig. 1)

Summary

Introduction

Kings and queens of eusocial termites can live for decades, while queens sustain a nearly maximal fertility. We observed an upregulated gene expression in fat bodies of reproductives of several components of the IIS pathway, including an insulin-like peptide, Ilp[9]. 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 understanding of the causes of aging stems to a large extent from studies on short-lived model organisms[11,12] Eusocial insects such as termites, ants and some bees and wasps seem to defy the trade-off between reproduction and longevity[13,14,15,16]. In long-lived termite kings, one expects the same, but the trade-off might need less bypassing if the reproductive investment is systematically lower than in queens

Methods

Results

Conclusion