The regulation of transposable element (TE) activity by small RNAs is a ubiquitous feature of germlines. However, despite the obvious benefits to the host in terms of ensuring the production of viable gametes and maintaining the integrity of the genomes they carry, it remains controversial whether TE regulation evolves adaptively. We examined the emergence and evolutionary dynamics of repressor alleles after P-elements invaded the Drosophila melanogaster genome in the mid-twentieth century. In many animals including Drosophila, repressor alleles are produced by transpositional insertions into piRNA clusters, genomic regions encoding the Piwi-interacting RNAs (piRNAs) that regulate TEs. We discovered that ∼94% of recently collected isofemale lines in the Drosophila melanogaster Genetic Reference Panel (DGRP) contain at least one P-element insertion in a piRNA cluster, indicating that repressor alleles are produced by de novo insertion at an exceptional rate. Furthermore, in our sample of approximately 200 genomes, we uncovered no fewer than 80 unique P-element insertion alleles in at least 15 different piRNA clusters. Finally, we observe no footprint of positive selection on P-element insertions in piRNA clusters, suggesting that the rapid evolution of piRNA-mediated repression in D. melanogaster was driven primarily by mutation. Our results reveal for the first time how the unique genetic architecture of piRNA production, in which numerous piRNA clusters can encode regulatory small RNAs upon transpositional insertion, facilitates the nonadaptive rapid evolution of repression.

中文翻译：

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piRNA介导的入侵转座因子沉默的快速进化是由大量的从头突变引起的。

小RNA对转座因子（TE）活性的调节是种系的普遍特征。然而，尽管在确保活体配子的产生和维持它们携带的基因组的完整性方面对宿主有明显的好处，但TE调控是否能自适应地发展仍存在争议。我们研究了20世纪中叶P元素入侵果蝇果蝇基因组后，阻遏性等位基因的出现和进化动力学。在包括果蝇在内的许多动物中，阻遏性等位基因是通过转位插入piRNA簇产生的，piRNA簇是编码调节TEs的Piwi相互作用RNA（piRNA）的基因组区域。我们发现果蝇遗传参考专家组（DGRP）中最近收集到的约94％的异种雌性品系在piRNA簇中至少包含一个P元素插入，这表明阻遏基因由反义插入以异常高的速率产生。此外，在我们大约200个基因组的样本中，我们在至少15个不同的piRNA簇中发现了不少于80个独特的P元素插入等位基因。最后，我们没有观察到piRNA簇中P元素插入的阳性选择的足迹，这表明piRNA介导的黑腹果蝇抑制的快速进化主要是由突变驱动的。我们的研究结果首次揭示了piRNA产生的独特遗传结构，其中许多piRNA簇在转座插入后可以编码调控性小RNA，