Highlights d Toxin-antidote elements (TAs) are present in all known Caenorhabditis selfing species d slow-1/grow-1 is a novel TA that causes developmental delay in C. tropicalis d TAs can antagonize each other, leading to more stable genetic incompatibilities

Horizontal gene transfer, the movement of genetic material between species, has been reported across all major eukaryotic lineages. However, the underlying mechanisms of transfer and their impact on genome evolution are still poorly understood. While studying the evolutionary origin of a selfish element in the nematode Caenorhabditis briggsae , we discovered that Mavericks , ancient virus-like transposons related to giant viruses and virophages, are one of the long-sought vectors of horizontal gene transfer. We found that Mavericks gained a novel herpesvirus-like fusogen in nematodes, leading to the widespread exchange of cargo genes between extremely divergent species, bypassing sexual and genetic barriers spanning hundreds of millions of years. Our results show how the union between viruses and transposons causes horizontal gene transfer and ultimately genetic incompatibilities in natural populations.