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Herein, we observed a range of age\u2010related modifications in testicular morphology and spermatogenic cells, and conducted single\u2010cell RNA sequencing on young and old testes in <jats:italic>Drosophila<\/jats:italic>. Pseudotime trajectory revealed significant changes in germline subpopulations during ageing. Our examination unveiled that genes showing bias in spermatids exhibited higher dN\/dS than those in GSCs_Spermatogonia. Genes biased towards young GSCs_Spermatogonia displayed higher dN\/dS than those in old GSCs_Spermatogonia. Interestingly, genes biased towards young spermatids demonstrated lower dN\/dS in contrast to those in old spermatids, revealing the complexity of evolutionary adaptations during ageing. Furthermore, mitochondria associated events, including oxidative phosphorylation, TCA cycle and pyruvate metabolism, were significantly enriched in germline subpopulations. Specifically, mitochondrial function was significantly impaired during the process of testicular ageing, concurrently emphasising the role of several key nuclear genome\u2010encoded mitochondrial regulatory genes, such as Hsp60B, fzo, Tim17b1 and mRpL12. 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