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In this study, Jansen et al. use a Drosophiladysgenesis model to demonstrate that tolerance thresholds to DNA damage constitute a crucial protective mechanism for maintaining germline genomic integrity and germ cell survival. They show that DNA double-strand breaks (DSBs) induced by P-element transposition cause mitotic germ cell loss through the activation of a CHK2 checkpoint and in a DSB dose-dependent manner, while postmitotic germ cells have higher DSB tolerance and progress further through oogenesis.