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

Abstract

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 of the possible causes underlying this phenomenon could be related to the high content of transposable elements (TE) in the Y chromosome (toxic Y hypothesis). TE activity is normally repressed by epigenetic mechanisms, but this regulation weakens with age. Since the Y chromosome is rich in TEs, age-related TE activity should be more pronounced in old males than in old females, likely affecting longevity patterns. In this work, we studied the natural variation in SGL in wild-type populations of three different Drosophila species that vary in their TE content: Drosophila melanogaster, Drosophila simulans, and Drosophila suzukii. Transcriptomic data revealed increased copy-specific TE expression in D. melanogaster and D. suzukii older flies. Moreover, we observed a higher number of upregulated TEs in old males compared to old 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 contributes to a better understanding of the genomic differences that lead to variation in longevity patterns between sexes in several species, and emphasizes the importance of studying the role of TEs in male longevity.