Transcriptomic evidence that insulin signalling pathway regulates the ageing of subterranean termite castes

Abstract

Insulin is a protein hormone that controls the metabolism of sugar, fat and protein via signal transduction in cells, influencing growth and developmental processes such as reproduction and ageing. From nematodes to fruit flies, rodents and other animals, glucose signalling mechanisms are highly conserved. Reproductive termites (queens and kings) exhibit an extraordinarily long lifespan relative to non-reproductive individuals such as workers, despite being generated from the same genome, thus providing a unique model for the investigation of longevity. The key reason for this molecular mechanism, however, remains unclear. To clarify the molecular mechanism underlying this phenomenon, we sequenced the transcriptomes of the primary kings (PKs), primary queens (PQs), male (WMs) and female (WFs) workers of the lower subterranean termite Reticulitermes chinensis. We performed RNA sequencing and identified 33 insulin signalling pathway-related genes in R. chinensis. RT-qPCR analyses revealed that EIF4E and RPS6 genes were highly expressed in WMs and WFs workers, while mTOR expression was lower in PKs and PQs than in WMs and WFs. PQs and PKs exhibited lower expression of akt2-a than female workers. As the highly conserved insulin signalling pathway can significantly prolong the healthspan and lifespan, so we infer that the insulin signalling pathway regulates ageing in the subterranean termite R. chinensis. Further studies are recommended to reveal the biological function of insulin signalling pathway-related genes in the survival of termites to provide new insights into biomolecular homeostasis maintenance and its relationship to remarkable longevity.

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

“…We propose that the IIS pathway, including the Ilp9 gene, activates the eIF6-crc gene program in the fat body of mature queens and kings. This in turn increases the synthesis of proteins involved in lipid synthesis and essential for fecundity, despite a downregulation of the TORC1 signaling pathway elsewhere described as the main pathway for protein synthesis 56 and also downregulated in whole bodies of reproductives of lower termite species 21,22 .…”

“…Recently, transcriptomic studies in different taxa of social insects have pointed out the importance of downstream components of the Insulin/insulin-like growth factor (IGF-1) signaling (IIS) and target of rapamycin (TOR) network for aging [20][21][22] . IIS and TOR signaling have been broadly identified as key actors in the allocation of resources and aging of organisms .…”

Why and how do termite kings and queens live so long?

“…TOR in termites as in other organisms. In addition, 4-year-old reproductives of the termite R. chinensis expressed significantly lower levels of the mTOR, eIF4, and RPS6 genes involved in TOR signalling and IIS than did workers, suggesting that long-lived reproductives may downregulate these growth signals [50]. In general, these nutrient-sensing growth pathways effect juvenile hormone (JH) production followed by upregulation of vitellogenin (Vg), a yolk protein required for egg production [90,91].…”

Eusociality and Senescence: Neuroprotection and Physiological Resilience to Aging in Insect and Mammalian Systems

“…Eusocial insect worker and reproductive castes differ in metabolism, and metabolic pathways may correlate with aging phenotypes (Corona et al, 2007;Ihle et al, 2019;Haroon, Ma et al, 2020). Caloric restriction has a positive effect on lifespan and senescence in humans (Most et al, 2017), some genetic strains of mice (Weindruch, 1992;Liao et al, 2010) and Drosophila (Burger et al, 2010), suggesting that by lowering metabolic activity cells form fewer injurious metabolites (Speakman and Mitchell, 2011).…”