Long-lived termite kings and queens activate telomerase in somatic organs

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.

Complex regulatory role of DNA methylation in caste- and age-specific expression of a termite

“…In M. natalensis , for instance, which is the focus of the current study, sterile workers live only weeks, while kings and queens can live for over 20 years [ 17 ], with the highly fertile queen laying thousands of eggs per day [ 18 ]. Several important genes and pathways have been indicated as important for longevity and fecundity in termites and other eusocial insects, such as the nutrient-sensing pathways Insulin/insulin-like growth factor (IGF-1) signalling (IIS) and target of rapamycin (TOR) [ 16 , 19 , 20 ], telomerase [ 21 ], transposon defence [ 16 , 22 ], oxidative stress [ 16 , 20 , 23 ], DNA damage repair and mitochondrial functions [ 20 , 23 ] Further, recent studies have also presented evidence for the transcriptional regulation of specific gene co-expression modules associated with old but highly fertile queens in ants [ 24 ], bees [ 25 ] and termites [ 20 , 26 , 27 ]. However, the role of DNA methylation in this absence of the longevity–fecundity trade-off in eusocial insects is so far unknown.…”

Telomerase as a possible key to bypass reproductive cost

“…In contrast to the common expectation, no telomere length decline was observed in old individuals of this species, along with declines in other physiological systems such as stress response and immune function; instead, all the tested parameters improved their efficiencies with age (Sauer et al 2021). ( 5) It is well-known that the fertility rate of termite queens increases with age along with their body mass, which, based on the evidence shown above, appears to be consistent with their increasing somatic telomerase activity (Adams and Atkinson 2008;Nozaki and Matsuura 2019;Koubová et al 2021a).…”

“…The common presumption that telomerase activity is a marker of aging and advancing organismal development, even in insects, is supported by observations in hemimetabolous insects such as cockroaches and termites (Korandová et al 2014;Koubová et al 2021a). Hemimetabolous insects exhibit incomplete metamorphosis, where ontogenetic development lacks larval and pupal stages and instead includes several nymphal stages that eventually molt into adults.…”

“…Both cockroaches and termites exhibit upregulated telomerase activity in young instars, which gradually declines during development. However, there were two exceptions for the decline: germline cells in both insects and somatic tissues in the long-lived reproductives (Korandová et al 2014;Koubová et al 2021a). Telomerase activity is also increased in adult somatic tissues of long-lived honeybee queens (Korandová and Frydrychová 2016;Koubová and Čapková Frydrychová 2021) and ant queens (our unpublished data), both of which are holometabolous insects with adult growth largely determined by metamorphosis.…”

“…Similarly, somatic telomerase activity is proposed for all species with indeterminate growth, including fungal mycelium, meristematic plant tissue, various invertebrate species, reptiles, amphibia, and fish (Klapper et al 1998a, b;Gomes et al 2010;Gruber et al 2014). Furthermore, numerous studies have shown that telomerase activity is unrelated to telomere length, as reviewed in Smith et al (2021), or that it remains constant or increases with age in animal species with both determinate and indeterminate growth (Francis et al 2006;Hartmann et al 2009;Anchelin et al 2011;Hoelzl et al 2016;Korandová and Frydrychová 2016;Koubová et al 2021a;Sauer et al 2021). Finally, telomerase and telomere length can be regulated by environmental factors such as stress exposure or seasonal effects (Entringer et al 2011;Young et al 2013;Rollings et al 2014;Mu et al 2015;Koubová et al 2021b;Smith et al 2021).…”