Why don't tissue maintain homeostasis forever? In Drosophila, testis homeostasis is maintained by the balance of self-renewal and differentiation in germline stem cells (GSCs) and cyst stem cells (CySCs).At the tip of adult testis, each GSC is surrounding by a pair of CySCs, which act non-autonomously to maintain GSC self-renewal.Here, we show that mating leads testes accumulated progenitors of both germ cells and cyst cells at the expense of spermatocyte and differentiated cyst cells.We find that it is resulted from hyperactivation of JNK signaling in the CySCs,leading to sustained transcription of self-renew factor-Zfh-1 in the CySC lineage.The ectopic CySC-like cells non-autonimously disrupted germ cell differentiation, leading to sterility of aged male.These defects were not found in testes from non-mated aged males, indicating that it is induced by mating.Furthermore, we find that knockdown of JNK phosphatase Puckered (Puc) in CySCs leads to massive CySC-like cell formation in testes from non-mated young males.Together, our results show that suppresion of JNK signaling in CySCs by Puc is essential to maintain balance between self-renewal and differentiation, and hyperactivation of JNK signaling by mating leads to loss of tissue homeostasis in aged male gonad.