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

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

Heritable effects on caste determination and colony-level sex allocation in termites under field conditions

The ecological success of social insects is attributed to the division of labor, where newly hatched offspring differentiate into either fertile progeny or functionally sterile worker castes. There is growing evidence for the heritable (genetic or epigenetic) effects on caste determination based on laboratory experiments. Here, we indirectly demonstrate that heritable factors have the principal role in caste determination and strongly affect colony-level production of both sexes of fertile dispersers (i.e., alates) in field colonies of the termite Reticulitermes speratus. An egg-fostering experiment suggests that the colony-dependent sex-specific caste fates were almost entirely determined before oviposition. Our investigation of field colonies revealed that such colony-dependent sex-specific caste fates result in the intercolonial variation in the numerical sex ratio of differentiated fertile offspring and, eventually, that of alates. This study contributes to better understanding the mechanisms underlying the division of labor and life-history traits in social insects

Plastic brain structure changes associated with the division of labour and ageing in termites

Division of labour is a prominent feature of social insect societies, where different castes engage in different specialised tasks. As brain differences are associated with behavioural differences, brain anatomy may be linked to caste polymorphism. Here, we show that termite brain morphology changes markedly with caste differentiation and age in the termite, Reticulitermes speratus. Brain morphology was shown to be associated with reproductive division of labour, with reproductive individuals (alates and neotenic reproductives) having larger brains than non-reproductives (workers and soldiers). Micro-computed tomography (CT) imaging and dissection observations showed that the king's brain morphology changed markedly with shrinkage of the optic lobes during their long life in the dark. Behavioural experiments showed that mature primary kings lose visual function as a result of optic lobe shrinkage. These results suggested that termites restructure their nervous systems to perform necessary tasks as they undergo caste differentiation, and that they also show flexible changes in brain morphology even after the final moult. This study showed that brain morphology in social insects is linked to caste and ageing, and that the evolution of the division of labour is underpinned by the development of diverse neural systems for specialised tasks. This article is protected by copyright. All rights reserved

The royal food of termites shows king and queen specificity

シロアリの王と女王の特別食を世界初解明 --王と女王の繁殖と長寿を支えるロイヤルフード--. 京都大学プレスリリース. 2023-07-13.Society in eusocial insects is based on the reproductive division of labor, with a small number of reproductive individuals supported by a large number of non-reproductive individuals. Because inclusive fitness of all colony members depends on the survival and fertility of reproductive members, sterile members provide royals with special treatment. Here we show that termite kings and queens each receive special food of a different composition from workers. Sequential analysis of feeding processes demonstrated that workers exhibit discriminative trophallaxis, indicating their decision-making capacity in allocating food to the kings and queens. LC-MS/MS analyses of the stomodeal food and midgut contents revealed king- and queen-specific compounds including diacylglycerols and short-chain peptides. DESI-MSI analyses of ¹³C-labelled termites identified phosphatidylinositol and acetyl-L-carnitine in the royal food. Comparison of the digestive tract structure showed remarkable differences in the volume ratio of the midgut-to-hindgut among castes, indicating that digestive division of labor underlies reproductive division of labor. Our demonstration of king- and queen-specific food in termites provides insight into the nutritional system that underpins the extraordinary reproduction and longevity of royals in eusocial insects

An Efficient Antioxidant System in a Long-Lived Termite Queen.

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

Long-Lived Termite Queens Exhibit High Cu/Zn-Superoxide Dismutase Activity

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

Dataset S1 from King- and queen-specific degradation of uric acid contributes to reproduction in termites

Caste-based reproductive division of labour in social insects is built on asymmetries in resource allocation within colonies. Kings and queens dominantly consume limited resources for reproduction, while non-reproductive castes such as workers and soldiers help reproductive castes. Studying the regulation of such asymmetries in resource allocation is crucial for understanding the maintenance of sociality in insects, although the molecular background is poorly understood. We focused on uric acid, which is reserved and used as a valuable nitrogen source in wood-eating termites. We found that king- and queen-specific degradation of uric acid contributes to reproduction in the subterranean termite Reticulitermes speratus. The urate oxidase gene (RsUAOX), which catalyses the first step of nitrogen recycling from stored uric acid, was highly expressed in mature kings and queens, and upregulated with differentiation into neotenic kings/queens. Suppression of uric acid degradation decreased the number of eggs laid per queen. Uric acid was shown to be provided by workers to reproductive castes. Our results suggest that the capacity to use nitrogen, which is essential for the protein synthesis required for reproduction, maintains to colony cohesion expressed as the reproductive monopoly held by kings and queens

Supplementary Materials from King- and queen-specific degradation of uric acid contributes to reproduction in termites

Text S1: Supplementary Materials and Methods; Figure S1; Table S1 and S