Gene regulation in the germline ensures the production of high-quality gametes, long-term maintenance of the species and speciation. Male germline transcriptomes undergo dynamic changes after the mitosis-to-meiosis transition and have been subject to evolutionary divergence among mammals. However, the mechanisms underlying germline regulatory divergence remain undetermined. Here, we show that endogenous retroviruses (ERVs) influence species-specific germline transcriptomes. After the mitosis-to-meiosis transition in male mice, specific ERVs function as active enhancers to drive germline genes, including a mouse-specific gene set, and bear binding motifs for critical regulators of spermatogenesis, such as A-MYB. This raises the possibility that a genome-wide transposition of ERVs rewired germline gene expression in a species-specific manner. Of note, independently evolved ERVs are associated with the expression of human-specific germline genes, demonstrating the prevalence of ERV-driven mechanisms in mammals. Together, we propose that ERVs fine-tune species-specific transcriptomes in the mammalian germline.

种系中的基因调控可确保生产高质量配子，长期维持物种和物种形成。男性生殖系转录组在有丝分裂到减数分裂过渡后发生动态变化，并在哺乳动物之间经历进化差异。但是，种系调节差异的潜在机制仍未确定。在这里，我们表明内源性逆转录病毒（ERVs）影响物种特定的种系转录组。在雄性小鼠的有丝分裂到减数分裂过渡后，特定的ERVs作为主动增强子来驱动种系基因（包括小鼠特异性基因集），并带有精子发生关键调节因子（如A-MYB）的结合基序。这增加了ERV的全基因组转座以种特异性方式重新连接种系基因表达的可能性。值得注意的是，独立进化的ERV与人类特异性种系基因的表达相关，证明了ERV驱动的机制在哺乳动物中盛行。在一起，我们建议ERVs调整哺乳动物种系中物种特定的转录组。