Longevity and transposon defense, the case of termite reproductives: in termites, kings’ and queens’ genomes are protected from genomic parasites; workers, not so much, and as a result they face premature aging.

Social insects such as honey bees or termites are promising new models for aging research. In contrast to short-lived models like the fruit fly or mouse, the reproductives of an insect colony have exceptionally long lifespans. This offers important new avenues for gerontology, especially as mechanisms underlying aging are highly conserved among animals. We studied aging in a termite from the wild. Our results suggest that aging in this species, as in other animals, is related to the activity of transposable elements (TEs; also known as ?jumping genes?). Yet reproductives seem to be protected by a process that normally silences TEs in the germline of animals. This suggests that natural selection used a mechanism from the germline to protect whole animals. Social insects are promising new models in aging research. Within single colonies, longevity differences of several magnitudes exist that can be found elsewhere only between different species. Reproducing queens (and, in termites, also kings) can live for several decades, whereas sterile workers often have a lifespan of a few weeks only. We studied aging in the wild in a highly social insect, the termite Macrotermes bellicosus , which has one of the most pronounced longevity differences between reproductives and workers. We show that gene-expression patterns differed little between young and old reproductives, implying negligible aging. By contrast, old major workers had many genes up-regulated that are related to transposable elements (TEs), which can cause aging. Strikingly, genes from the PIWI-interacting RNA (piRNA) pathway, which are generally known to silence TEs in the germline of multicellular animals, were down-regulated only in old major workers but not in reproductives. Continued up-regulation of the piRNA defense commonly found in the germline of animals can explain the long life of termite reproductives, implying somatic cooption of germline defense during social evolution. This presents a striking germline/soma analogy as envisioned by the superorganism concept: the reproductives and workers of a colony reflect the germline and soma of multicellular animals, respectively. Our results provide support for the disposable soma theory of aging.


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