Mosquito genomes are frequently invaded by transposable elements through horizontal transfer

Author summary A large fraction of most eukaryotic genomes is derived from DNA fragments that can multiply by inserting themselves in other regions of the genome, generating genomic instability and variability. These fragments are called Transposable Elements (TEs). Since they are a constituent part of the eukaryote genomes, these DNA pieces are normally inherited vertically along with other genes to the host offspring. Host genomes have an arsenal of molecular mechanisms that were naturally selected to control TEs replication avoiding most deleterious damage to the genome and hence leading to long-term TEs inactivation and degeneration. However, TEs sometimes get out of control and invade other species through horizontal transfer, the transfer of genetic information through other means than sexual intercourse. This phenomenon is poorly studied in mosquitoes, a highly important Insect taxa that transmit many human pathogens. We characterized the whole TE content of 24 mosquito genomes and investigated the TE inheritance mode uncovering hundreds of horizontal transfer events among these species and distantly related ones. We also identify a mosquito parasitic filarial worm, that is involved as a transfer vector between many species of mosquitoes and that horizontally transferred TEs contributed significantly to mosquito's genome expansion and variation. Transposable elements (TEs) are mobile genetic elements that parasitize basically all eukaryotic species genomes. Due to their complexity, an in-depth TE characterization is only available for a handful of model organisms. In the present study, we performed a de novo and homology-based characterization of TEs in the genomes of 24 mosquito species and investigated their mode of inheritance. More than 40% of the genome of Aedes aegypti, Aedes albopictus, and Culex quinquefasciatus is composed of TEs, varying substantially among Anopheles species (0.13%-19.55%). Class I TEs are the most abundant among mosquitoes and at least 24 TE superfamilies were found. Interestingly, TEs have been extensively exchanged by horizontal transfer (172 TE families of 16 different superfamilies) among mosquitoes in the last 30 million years. Horizontally transferred TEs represents around 7% of the genome in Aedes species and a small fraction in Anopheles genomes. Most of these horizontally transferred TEs are from the three ubiquitous LTR superfamilies: Gypsy, Bel-Pao and Copia. Searching more than 32,000 genomes, we also uncovered transfers between mosquitoes and two different Phyla-Cnidaria and Nematoda-and two subphyla-Chelicerata and Crustacea, identifying a vector, the worm Wuchereria bancrofti, that enabled the horizontal spread of a Tc1-mariner element among various Anopheles species. These data also allowed us to reconstruct the horizontal transfer network of this TE involving more than 40 species. In summary, our results suggest that TEs are frequently exchanged by horizontal transfers among mosquitoes, influencing mosquito's genome size and variability.