Recurrent evolution of selfishness from an essential tRNA synthetase in Caenorhabditis tropicalis

No genome on Earth is free of selfish genes. This reflects both their ability to subvert the laws of inheritance and their de novo emergence from host genes. Yet, despite their ubiquity and key role in driving innovation, the mechanisms responsible for their genesis remain largely unexplored. Here we report the discovery of three toxin–antidote elements in the nematode Caenorhabditis tropicalis. Toxin–antidote elements are selfish genes that increase their frequency in populations by poisoning non-carrier individuals. We find that all three novel toxins—klmt-1, pzl-1 and hyde-1—arose via gene duplication from fars-3, an essential subunit of the phenylalanyl tRNA synthetase. Their antidotes—KSS proteins—are rapidly evolving F-box proteins that degrade toxins via the SCF ubiquitin–ligase complex. Our phylogenetic and genomic analyses strongly suggest that the ancestor of all extant KSS antidotes fortuitously acquired affinity for FARS-3, much like ‘self’ proteins are targeted in autoimmune disease. This interaction neutralized the toxicity of future paralogues before it arose (presuppression), allowing otherwise deleterious mutant alleles to persist and ultimately evolve into selfish genes—consistent with the theory of constructive neutral evolution.