Longevity and transposon defense, the case of termite reproductives

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 germlineof 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 germlineof animals can explain the long life of termite reproductives, implying somatic cooption of germlinedefense during social evolution. This presents a striking germline/ somaanalogy as envisioned by the superorganismconcept: the reproductives and workers of a colony reflect the germlineand somaof multicellular animals, respectively. Our results provide support for the disposable somatheory of aging.