How do termite queens and kings stay healthy for decades?

Reproductive and worker castes of termites differ greatly in their morphology and behavior but also in their fertility and longevity. Kings and queens of the highly social termite, Macrotermes natalensis, live for decades, with the queen laying thousands of eggs per day. Workers are sterile and only live a few weeks. In our HFSP project, we investigated the regulatory mechanisms involved in generating such diverse phenotypes. Our previous results indicate that well-regulated transcription allows reproductive castes to overcome simultaneously several well-known hallmarks of aging^1,2.

More recently, we observed that a large number of genes are associated with Transposable Elements (TEs) that are mobile sequences of DNA that can become transcriptionally active as an animal ages. The regulation of TEs for instance via the PIWI-pathway, is known to be an important mechanism to protect the integrity of genomes, especially in the germ-line where mutations can be transmitted to offspring. In social insects, soma and germ-line are divided among worker and reproductive castes, so one may expect caste-specific differences in TE regulation to exist. To test this, we compared whole-genome levels of repeat element transcription and our transcriptomic analyses in the fat body of female workers, kings, and five different queen stages of the Macrotermes natalensis. We found substantially higher TE activity in workers than in reproductives. Furthermore, relative TE expression decreased with age in queens, due to a significant upregulation of the PIWI pathway in 20-year-old queens. Our results suggest a caste- and age-specific regulation of the PIWI-pathway has evolved in higher termites that is analogous to germ-line-specific activity in individual organisms, promoting reproductive fitness even at high age.

1- Séité S., Harrison M. C., …. Vasseur-Cognet M. Lifespan prolonging mechanisms and insulin upregulation without fat accumulation in long-lived reproductives of a higher termite. Communications Biology, 2022; https://doi.org/10.1038/s42003-021-02974-6

2- Harrison M. C., Dohmen E., George S., Sillam-Dussès D., Séité S., Vasseur-Cognet M. Complex regulatory role of DNA methylation in caste- and age-specific expression of a termite. Open Biology, 2022; https://doi.org/10.1098/rsob.220047