Strong evidence for multiple horizontal transfers of immune genes between teleost fishes

Abstract Horizontal gene transfer (HGT) is less frequent in eukaryotes than in prokaryotes, yet can have strong functional implications and was proposed as causal factor for major adaptations in several eukaryotic lineages. Most cases of eukaryote HGT reported to date are inter-domain transfers and only few studies have investigated eukaryote-to-eukaryote HGTs. Furthermore, the extent to which HGT has contributed to the gene repertoire of some lineages such as vertebrates remains unclear. Here, we performed a large-scale survey of HGT among 242 species of ray-finned fishes. We found strong evidence supporting 18 teleost-to-teleost HGT events that involve 17 different genes in 11 teleost fish orders. The genes involved in these transfers show lower synonymous divergence than expected under vertical transmission, their phylogeny is inconsistent with that of teleost fishes, and high nucleotide similarity on these genes between donor and recipient lineages extends to non-coding regions. The distribution of HGT events in the teleost tree is heterogenous, with eight of the 18 transfers occurring between the same two orders (Osmeriformes and Clupeiformes). Besides the previously reported transfer of an antifreeze protein, most transferred genes play roles in immunity, suggesting that such genes are more likely than others to confer strong selective advantage to the recipient species. Overall, our work shows that teleost-to-teleost HGT has occurred on multiple occasions and it will be worth further quantifying these transfers and evaluating their impact on teleost evolution as more genomes are being sequenced.