Exploring the Role of Transposable Elements to Sex Gap in Longevity in Three Drosophila Species

ABSTRACT

In Drosophila , like other animal species, females tend to live longer than males, a phenomenon known as sex gap in longevity (SGL). One possible explanation could involve the activity of transposable elements (TE). TEs are normally repressed by epigenetic mechanisms, but this regulation weakens with age. Y chromosomes are enriched in TEs, and age‐related TE activity may therefore be more pronounced in older males, likely affecting longevity (toxic Y hypothesis). Using three Drosophila species with different TE content, we showed that SGL varies among wild‐type populations, reflecting both intra‐ and interspecies differences. Transcriptomic data revealed an age‐related increase in TE‐derived reads in D. melanogaster and D. suzukii , but not in D. simulans , with no differences between sexes. However, we observed a higher number of upregulated TE copies in older males compared to older females across the three species tested, which does not necessarily reflect increased transposition activity. Moreover, longevity assays did not reveal an association between increased TE expression and reduced lifespan. Finally, replacing the Y chromosome between strains with different SGL resulted in a progressive and strain‐specific reduction of male lifespan in D. melanogaster , despite similar Y chromosome size. This was accompanied by gene expression changes and increased TE expression. In summary, our work calls for a reconsideration of the toxic Y hypothesis, suggesting it may be less relevant in species with low genomic TE content. Notably, Y chromosome effects on lifespan seem to be driven more by Y‐linked heterochromatic polymorphisms and epistatic interactions than by overall TE abundance.