Evidence for an Ancient Bilaterian Origin of the RAG-Like Transposon

The Recombination Activating Genes (RAG1 and RAG2) of jawed vertebrates are thought to have evolved from a RAGL (RAG-like) transposon containing convergently oriented RAG1-like (RAG1L) and RAG2-like (RAG2L) genes. Elements resembling this presumptive evolutionary precursor have thus far only been detected convincingly in deuterostomes, leading to the model that the RAGL transposon first appeared in an early deuterostome. Here, we report the identification of numerous RAGL transposons in the genomes of protostomes, including oysters and mussels (phylum Mollusca) and ribbon worms (phylum Nemertea), and in the genomes of several cnidarians.  Phylogenetic analyses indicate that a RAGL transposon was present in an early bilaterian and that this transposon family evolved in a vertical manner within the Bilateria clade.   Many of the RAGL transposons detected in protostomes are intact elements containing convergently oriented RAG1L and RAG2L genes flanked by terminal inverted repeats and target site duplications with striking similarities with the corresponding elements in deuterostomes.  This, combined with the integrity of critical domains and amino acids, argues that some RAGL transposons might be active currently in the protostome clade.  Our findings indicate that the RAGL transposon arose earlier in evolution than previously thought, either in an early bilaterian or prior to the divergence of bilaterians and non-bilaterians, and have implications for our understanding of the evolutionary history of this important transposon family.