Abstract
Kings and queens of termites, like queens of other advanced eusocial insects, are endowed with admirable longevity, which dramatically exceeds the life expectancies of their non-reproducing nest-mates and related solitary insects. In the quest to find the mechanisms underlying the longevity of termite reproductives, we focused on somatic maintenance mediated by telomerase. This ribonucleoprotein is well established for pro-longevity functions in vertebrates, thanks primarily to its ability of telomere extension. However, its participation in lifespan regulation of insects, including the eusocial taxa, remains understudied. Here, we report a conspicuous increase of telomerase abundance and catalytic activity in the somatic organs of primary and secondary reproductives of the termite Prorhinotermes simplex and confirm a similar pattern in two other termite species. These observations stand in contrast with the telomerase downregulation characteristic for most adult somatic tissues in vertebrates and also in solitary insects and non-reproducing castes of termites. At the same time, we did not observe caste-specific differences in telomere lengths that might explain the differential longevity of termite castes. We conclude that although the telomerase activation in termite reproductives is in line with the broadly assumed association between telomerase and longevity, its direct phenotypic impact remains to be elucidated.
Highlights
The reproductive castes of advanced social insects are often very long-lived when compared with their non-reproducing nest-mates and solitary insect relatives
A significant increase in telomerase activity (TA) was recorded from the first days after the neotenic differentiation (F5,12 = 26.19, p < 10−4), and the maximum activity was observed in the soma of mature, 1-year-old neotenics (40 and 20 times higher in males and females, respectively, compared to workers; q(3,3) > 10.2 and p < 10−4 for both). Pr. simplex TERT (psTERT) expression roughly followed the trend of TA, without the final increase to peak values in 1-year-old reproductives. psTERT quantity showed a fluctuating trend, but consistently with the previous experiments, we observed its significant increase in 1-year-old neotenics, compared to workers
We demonstrated a strong association between the life expectancies of different castes and the somatic activation of telomerase
Summary
The reproductive castes of advanced social insects are often very long-lived when compared with their non-reproducing nest-mates and solitary insect relatives. In view of this assumption, we study here the telomerase mechanism in termites, with emphasis on the differences between the working stages and the reproductives during their maturation (first year) and maturity (3–5 years) To this goal, we characterize the gene and protein structure of Pr. simplex TERT (psTERT) from genomic and transcriptomic data, quantify the transcript and protein abundances of psTERT, study the enzymatic activity of telomerase and establish the lengths of telomeres. We characterize the gene and protein structure of Pr. simplex TERT (psTERT) from genomic and transcriptomic data, quantify the transcript and protein abundances of psTERT, study the enzymatic activity of telomerase and establish the lengths of telomeres Using these complementary methods, we try to cover the differences and dynamics in telomerase mechanism activation and telomere lengths in all developmental stages and castes, including both types of reproductives of both sexes and known ages, and in different organs.
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