Evolution of P element in eukaryotes and its domestication in vertebrates

P elements are a crucial component of DNA transposons, playing a vital role in shaping the evolution of eukaryotic genomes, yet their evolutionary profiles remain largely unknown. Here, we identified 1,801 P elements across 678 species, predominantly in Arthropods (578 species). Phylogenetic analysis revealed nine distinct families ( Bus , Cab , Car , Gig , Taxi , Rook , Dive , Che , and Coach ), each exhibiting distinct evolutionary trajectories. Despite considerable variation in transposon length, terminal inverted repeats, and flanking sequences, all families retain a highly conserved six-domain transposase architecture comprising the THAP DNA-binding domain (Thap), leucine zipper dimerization domain (LZDD), helix-turn-helix domain (HTH), RNase H-like catalytic domain (DDE), GTP-binding domain (GBD), and C-terminal domain (CTD), consistent with a “constrained core, variable periphery” evolutionary model. Kimura divergence analysis revealed contrasting evolutionary dynamics: the Bus , Coach , Car , and Dive families showed near-zero divergence peaks indicative of recent or ongoing transposition, whereas the Cab , Gig , and Taxi families represented remnants of ancient invasions, and the Che and Rook families exhibited multiple invasion waves. We further detected signatures of horizontal transfer in six families, including a striking cross-phylum transfer, indicating that horizontal transfer has repeatedly complemented vertical inheritance in the spread of P elements. Furthermore, we demonstrated that vertebrate Thap9 genes originated from a single domestication event of Che family transposases early in vertebrate evolution under strong purifying selection. Our findings establish a comprehensive classification framework for the P transposon superfamily, reveal family-specific evolutionary dynamics shaped by both vertical inheritance and horizontal transfer, and trace the origin of Thap9 domestication, providing new insights into the diversification, activity, and co-option of this major transposon lineage.