Reactive oxygen species (ROS) are generated spontaneously in all organisms and cause oxidative damage to biomolecules when present in excess. Accumulated oxidative damage accelerates aging; enhanced antioxidant capacity may be a positive factor for longevity. Recently, numerous studies of aging and longevity have been performed using short-lived animals, however, longevity mechanisms remain unknown. Here we show that a termite Reticulitermes speratus that is thought to be long-lived eusocial insect than other solitary insects uses large quantities of uric acid as an antioxidant against ROS. We demonstrated that the accumulation of uric acid considerably increases the free radical-scavenging activity and resistance against ultraviolet-induced oxidative stress in laboratory-maintained termites. In addition, we found that externally administered uric acid aided termite survival under highly oxidative conditions. The present data demonstrates that in addition to nutritional and metabolic roles, uric acid is an essential antioxidant for survival and contributes significantly to longevity. Uric acid also plays important roles in primates but causes gout when present in excess in humans. Further longevity studies of long-lived organisms may provide important breakthroughs with human health applications.

The trade-off between reproduction and longevity is known in wide variety of animals. Social insect queens are rare organisms that can achieve a long lifespan without sacrificing fecundity. The extended longevity of social insect queens, which contradicts the trade-off, has attracted much attention because it implies the existence of an extraordinary anti-aging mechanism. Here, we show that queens of the termite Reticulitermes speratus incur significantly lower oxidative damage to DNA, protein and lipid and have higher activity of antioxidant enzymes than non-reproductive individuals (workers and soldiers). The levels of 8-hydroxy-2’-deoxyguanosine (oxidative damage marker of DNA) were lower in queens than in workers after UV irradiation. Queens also showed lower levels of protein carbonyls and malondialdehyde (oxidative damage markers of protein and lipid, respectively). The antioxidant enzymes of insects are generally composed of catalase (CAT) and peroxiredoxin (Prx). Queens showed more than two times higher CAT activity and more than seven times higher expression levels of the CAT gene RsCAT1 than workers. The CAT activity of termite queens was also markedly higher in comparison with other solitary insects and the queens of eusocial Hymenoptera. In addition, queens showed higher expression levels of the Prx gene RsPRX6. These results suggested that this efficient antioxidant system can partly explain why termite queens achieve long life. This study provides important insights into the evolutionary linkage of reproductive division of labor and the development of queens’ oxidative stress resistance in social insects.

Lifespan varies greatly across the tree of life. Of the various explanations for this phenomenon, those that involve trade-offs between reproduction and longevity have gained considerable support. There is an important exception: social insect reproductives (queens and in termites, also kings) exhibit both high reproductive outputs and extraordinarily long lives. As both the ultimate and proximate mechanisms underlying the absence of the fecundity/longevity trade-off could shed light on the unexpected dynamics and molecular mechanisms of extended longevity, reproductives of social insects have attracted much attention in the field of ageing research. Here, we highlight current ecological and physiological studies on ageing and discuss the various possible evolutionary and molecular explanations of the extended lifespans of termite reproductives. We integrate these findings into a coherent framework revealing the evolution of longevity in these reproductives. Studies on termites may explain why and how ageing is shaped by natural selection. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

In most organisms, superoxide dismutases (SODs) are among the most effective antioxidant enzymes that regulate the reactive oxygen species (ROS) generated by oxidative energy metabolism. ROS are considered main proximate causes of aging. However, it remains unclear if SOD activities are associated with organismal longevity. The queens of eusocial insects, such as termites, ants, and honeybees, exhibit extraordinary longevity in comparison with the nonreproductive castes, such as workers. Therefore, the queens are promising candidates to study the underlying mechanisms of aging. Here, we found that queens have higher Cu/Zn‐SOD activity than nonreproductive individuals of the termite Reticulitermes speratus. We identified three Cu/Zn‐SOD sequences and one Mn‐SOD sequence by RNA sequencing in R. speratus. Although the queens showed higher Cu/Zn‐SOD activity than the nonreproductive individuals, there were no differences in their expression levels of the Cu/Zn‐SOD genes RsSOD1 and RsSOD3A. Copper (Cu²⁺ and Cu⁺) is an essential cofactor for Cu/Zn‐SOD enzyme activity, and the queens had higher concentrations of copper than the workers. These results suggest that the high Cu/Zn‐SOD activity of termite queens is related to their high levels of the cofactor rather than gene expression. This study highlights that Cu/Zn‐SOD activity contributes to extraordinary longevity in termites.

Extreme conditions are normal for animals living in harsh environments. These animals adapt to their habitats and can use difficult conditions by default. Organisms living in enclosed spaces, notably termites in decaying wood, experience low O₂and high CO₂gas conditions due to limited gas exchange and high insect density. Termite queens, in particular, reproduce in royal chambers deep inside the wood, wherein tens of thousands of individuals engage in social labour. Here, we demonstrate that royal chambers in termite nests have low O₂and high CO₂gas concentrations, which enhance egg production by queens. We identified a unique gas condition of royal chambers in the nest of the subterranean termiteReticulitermes speratus, which is characterized by low O₂(15.75%) and high CO₂(4.99%) concentrations. Queens showed significantly greater fecundity under the low O₂and high CO₂gas conditions in the royal chambers than under ambient gas conditions. Quantitative PCR analysis revealed that the royal chamber gas conditions significantly promoted the expression levels of the vitellogenin genesRsVg1,RsVg2andRsVg3in queens compared with ambient gas conditions. This study highlights the adaptation of animals that live in closed habitats, which are hypoxic and hypercapnic as the result of their own metabolism, so as to have a high fitness in such environmental conditions.