Abstract
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.
Highlights
The key character of eusociality is reproductive division of labor within collaborative groups
To investigate whether high resistance to oxidative stress allows termite queens to achieve long lifespan, we performed a comparison of oxidative damage to biomolecules in R. speratus queens and workers (Fig 1A)
We assessed the levels of oxidative lipid damage in queens and workers using a thiobarbituric acid reactive substances (TBARS) assay, which is a well-established method for screening for malondialdehyde (MDA), the end product of lipid peroxidation [33, 34]
Summary
The key character of eusociality is reproductive division of labor within collaborative groups. Social species such as ants, honeybees, and termites have a one or a limited number of individuals that produce most or all of the offspring (queens), and a large number of individuals that forego reproduction for group beneficial activities (workers). In these insects, queens live up to 10 times longer than non-reproductive workers [1,2,3,4]. Longevity is typically negatively correlated with fecundity and the extent of this trade-off varies within and among species [5].
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