Transposable Elements and the Impact of Genomic Autoimmunity

Transposable elements (TEs), originally characterized in maize, are ubiquitous features of eukaryotes and replicate within genomes independent of the host replication cycle. This replicative advantage can result in genomes that are almost entirely composed of these selfish genetic elements. Most mutations caused by TE insertions are harmful, and all eukaryotes have evolved mechanisms to limit TE replication. This process requires the careful distinction between self and nonself, or host versus TE. Eukaryotic genome defense commonly relies on Argonaute proteins that block the TE replication cycle, guided by small RNAs that detect harmful TE transcripts. Because no system of immunity is perfect, genes can be caught in the crossfire and inappropriately silenced. Here, mainly focusing on maize and Drosophila, we discuss how off-target small RNA silencing can arise. This genomic immunity can shape TE evolutionary dynamics, establish novel modes of adaptation and epigenetic inheritance, and establish evolutionary feedback that shapes the evolution of gene silencing itself.