Pinpointing the vesper bat transposon revolution using the Miniopterus natalensis genome

Roy N. Platt, Sarah F. Mangum, David A. Ray

Around 40 million years ago DNA transposons began accumulating in an ancestor of bats in the family Vespertilionidae. Since that time, Class II transposons have been continuously reinvading and accumulating in vespertilionid genomes at a rate that is unprecedented in mammals. Miniopterus (Miniopteridae), a genus of long-fingered bats that was recently elevated from Vespertilionidae, is the sister taxon to the vespertilionids and is often used as an outgroup when studying transposable elements in vesper bats. Previous wet-lab techniques failed to identify Helitrons, TcMariners, or hAT transposons in Miniopterus. Limitations of those methods and ambiguous results regarding the distribution of piggyBac transposons left some questions as to the distribution of Class II elements in this group. The recent release of the Miniopterus natalensis genome allows for transposable element discovery with a higher degree of precision. Here we analyze the transposable element content of M. natalensis to pinpoint with greater accuracy the taxonomic distribution of Class II transposable elements in bats. These efforts demonstrate that, compared to the vespertilionids, Class II TEs are highly mutated and comprise only a small portion of the M. natalensis genome. Despite the limited Class II content, M. natalensis possesses a limited number of lineage-specific, low copy number piggyBacs and shares several TcMariner families with vespertilionid bats. Multiple efforts to identify Helitrons, one of the major TE components of vesper bat genomes, using de novo repeat identification and structural based searches failed. These observations combined with previous results inform our understanding of the events leading to the unique Class II element acquisition that characterizes vespertilionids. While it appears that a small number of TcMariner and piggyBac elements were deposited in the ancestral Miniopterus + vespertilionid genome, these elements are not present in M. natalensis genome at high copy number. Instead, this work indicates that the vesper bats alone experienced the expansion of TEs ranging from Helitrons to piggyBacs to hATs.