Telomerase is upregulated in the long-lived eusocial
reproductives
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. Recent phylogenetic studies indicate that
termites evolved from cockroaches, and along with cockroaches, they form
the order Blattodea (Inward et al. 2007). But, in contrast to
cockroaches, termites are eusocial insects. 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Koubová and Čapková Frydrychová 2021) and ant queens (our unpublished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. These findings suggest that
telomerase upregulation is important in caste differentiation in
eusocial insects (both holometabolous and hemimetabolous) and in the
extended longevity of their reproductive individuals.
It is well established that where telomerase is required for the
maintenance of telomeres, it is active during DNA replication stage
(S-phase), and while high levels of telomerase activity are found in
S-phase, telomerase activity is virtually absent in G2/M or G0 phases
(Zhu et al. 1996; Holt et al. 1997). Surprisingly, no DNA synthesis was
detected in telomerase-positive somatic tissues of honeybee queens
(Koubová and Čapková Frydrychová 2021) or the termiteProrhinotermes simplex (our unpublished data). Furthermore, there
were no differences in telomere length between the long-lived and
short-lived castes of honeybees or the tested ant (Lasius niger )
or termite (P. simplex ) (Jemielity et al. 2007; Korandová and
Frydrychová 2016).
To explain the role of telomerase in the caste system of eusocial
insects and to identify its possible engagement in the disparity between
fertility and life expectancy, research was further conducted examining
the bumblebee Bombus terrestris (Koubová et al. 2019). Bumblebees
are members of the group of insects possessing a primitive social
organization, and there are significant differences in the life
expectancies of their female castes. Workers of the bumblebee speciesB. terrestris typically live for 2-3 months, however, the queens
can live up to one year. Nevertheless, the lifespan comparison is not
unbiased, as bumblebee queens spend the majority of their lives
(approximately 6-9 months) in diapause, in which most biological
processes take place at only low-cost levels. Thus, bumblebee queens
cannot provide an example of a full-bodied extension of life expectancy,
or at least they cannot provide it in the way that exists in advanced
eusocial species. In contrast to eusocial reproductive individuals, the
only adult somatic tissue of B. terrestris showing upregulated
telomerase was the fat body of very young and pre-diapause queens
(Koubová et al. 2019). Additionally, telomerase activity in fat body was
co-localized with the DNA endoreduplication cycles that were followed by
a massive increase in fat body mass and nutrient content, which suggests
that the upregulation of telomerase activity in the fat body is tightly
linked to the ability of queens to survive upcoming diapause (Koubová et
al. 2019). A similar observation was obtained in honeybee workers, where
telomerase activity, DNA synthesis, and nutrient content were reinforced
in the fat body cells of winter-generation workers (Koubová et al.
2021b).
As there is very little cell turnover or DNA synthesis in most adult
insect soma, we can expect that the caste-related differences in
telomerase activity in eusocial insects such as honeybees or termites
are not linked to telomere maintenance mechanisms, and instead, they can
be associated with some non-canonical telomerase role, i.e. a role of
telomerase without the typical telomerase catalytic activity that
directly serves to elongate telomeres.