In Drosophila germlines, piRNA pathway collaborate with other piRNA effector proteins to generate piRNAs and act as an immune system that regulates transposable elements (TEs). The piRNA pathway is proposed to adapt to changes in genomic TEs by changing the composition of the piRNA pool. However, several piRNA pathway proteins exhibit signatures of positive selection along the linages leading to Drosophila melanogaster and D. simulans. To understand what drives these adaptive changes, we performed interspecific complementation, comparing the ability of D. simulans and D. mlenaogaster wild-type alleles to complement a D. melanogaster mutant background on three adaptively evolving piRNA pathway proteins: Armitage (Armi), Aubergine (Aub) and Spindle-E (SpnE). We observed that D. simulans alleles of aub and armi, exhibited defects in both piRNA ping-pong biogenesis and phased biogenesis. Surprisingly, the piRNA biogenesis defects of D. simulans alleles did not translate to TE deregulation. Furthermore, we found that D. simulans alleles were associated with increased off-target events of piRNA-mediated silencing, supporting the genomic autoimmunity hypothesis that specificity of the piRNA machinery drives the adaptive evolution of piRNA pathway proteins. Together, our results suggest that positive selection drove by the specificity of piRNA machinery has not targeted the ability of piRNA pathway proteins to regulate TE transcripts, but rather has acted on their functions in piRNA biogenesis.
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