Exploring the role of transposable elements to sex gap in longevity in Drosophila species

In Drosophila, like in many other animal species, females tend to live longer than males, a phenomenon known as sex gap in longevity (SGL). One possible explanation for this phenomenon could be related to the activity of transposable elements (TE), which may be present at higher levels in the heterogametic sex. TE activity is normally repressed by epigenetic mechanisms, but this regulation weakens with age. Sex chromosomes, such as the Y chromosome, are enriched in TEs, and age-related TE activity may therefore be more pronounced in older males than in older females, likely affecting longevity patterns. Using three Drosophila species, we show that SGL varies naturally among wild-type populations, reflecting both intra-and inter-species differences. Transcriptomic data revealed increased age-related TE expression in D. melanogaster and D. suzukii flies, but not in D. simulans. Moreover, we observed a higher number of upregulated TE copies in older males compared to older females across all the three species tested. Additionally, we detected an increase in TE-chimeric transcript generation in some aged samples, particularly in D. suzukii males. Finally, the replacement of the Y chromosome between strains with different SGL led to a progressive reduction in male lifespan and increased TE transcriptional release over generations, suggesting a Y chromosome important role in male longevity. Our work highlights the importance of investigating the role of TEs to better understand differences in longevity between sexes and across different species.