Longevity and transposon defence, the case of termite queens

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Organisms age but they do so at different pace. What causes ageing is a major question of fundamental importance for scientists and the general public alike. Work on model organisms, such as the nematode Caenorhabditis elegans, the fly Drosophila melanogaster, or mice, reveal important insights into the mechanisms underlying ageing. Yet, more recently studies outside these r-selected laboratory species are requested to address ageing under natural conditions and for species with different life histories. Social insects, like the honeybee, ants and termites, are promising new avenues for ageing research. Within a single colony, nestmates that share the same genetic background can differ by two orders of magnitude in lifespan. While the reproducing queens (and in termites also kings) live for more than 20 years, workers often have a lifespan of a few months only. Outside of social insects similar large differences in rates of ageing are only found between widely divergent species, where comparisons are far more difficult. Studying a highly social termite, Macrotermes bellicosus, we recently uncovered that a mechanism, which normally protects the germline of animals against ageing, might explain these longevity differences between castes. Old termite workers were characterized by a high expression of transposable elements (TEs). Such 'jumping genes' can interfere with genome integrity and gene functioning and they have been associated with ageing in many animals, including humans. Queens and kings seem to be protected against TEs by the piRNA (PIWI-interacting RNA) pathway that normally protects the germline of animals against TE activity. While genes for this pathway were constantly highly expressed in queens and kings, they were downregulated in old workers. In the current project, we aim to analyse this TE-piRNA mechanism in more detail to test functional links. In Objective 1 we will improve the quality of the sequenced genome of the study species to obtain a high quality genome, especially suitable for TE analyses. Objective 2 mainly aims at testing the consequences of TE activity, namely whether they result in TE transposition at different sites within the genome. We will test this for two tissues in old workers. Finally, in Objective 3 we will test for a causal relationship between piRNA expression and (i) TE activity, (ii) TE transposition, and (iii) longevity by performing a RNA interference experiment against an essential piRNA gene in M. bellicosus queens. Our project will contribute towards a better understanding of the causes of ageing and longevity, especially as TE activity and the piRNA pathway have been recently discussed by gerontologists to be a major mechanistic cause of ageing that has largely been neglected.