A role for host–parasite interactions in the horizontal transfer of transposons across phyla

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Abstract
The horizontal transfer (HT) of genetic material between non-mating species, common in bacteria, is increasingly being recognized as a significant force in eukaryotic evolution. Most instances of HT described so far in metazoans involve mobile genetic elements — mainly transposons — but the mechanisms enabling this exchange between widely divergent species are unknown. Gilbert et al. now show that transposable elements spread between disparate species by hitch-hiking in the genomes of parasites shared by these species. Specifically, Rhodnius prolixus, an insect that feeds on the blood of tetrapods and which is the vector of Chagas disease in humans, carries four distinct transposon families in its genome that can invade the genomes of a range of tetrapods including the opossum and squirrel monkey. One of these transposon families is also present in the pond snail Lymnaea stagnalis, a vector of trematodes infecting many vertebrates. 'Horizontal gene transfer' refers to the passage of genetic material between non-mating species. Transposable elements (transposons) may be especially prone to horizontal gene transfer, but the mechanisms by which they can spread across diverged species have been elusive. Here it is shown that transposons can spread by hitchhiking in the genomes of parasites. The amount of DNA that can be transferred in this way underscores the impact of horizontal gene transfer on genome evolution. Horizontal transfer (HT), or the passage of genetic material between non-mating species, is increasingly recognized as an important force in the evolution of eukaryotic genomes1,2. Transposons, with their inherent ability to mobilize and amplify within genomes, may be especially prone to HT3,4,5,6,7. However, the means by which transposons can spread across widely diverged species remain elusive. Here we present evidence that host–parasite interactions have promoted the HT of four transposon families between invertebrates and vertebrates. We found that Rhodnius prolixus, a triatomine bug feeding on the blood of various tetrapods and vector of Chagas’ disease in humans, carries in its genome four distinct transposon families that also invaded the genomes of a diverse, but overlapping, set of tetrapods. The bug transposons are ∼98% identical and cluster phylogenetically with those of the opossum and squirrel monkey, two of its preferred mammalian hosts in South America. We also identified one of these transposon families in the pond snail Lymnaea stagnalis, a cosmopolitan vector of trematodes infecting diverse vertebrates, whose ancestral sequence is nearly identical and clusters with those found in Old World mammals. Together these data provide evidence for a previously hypothesized role of host–parasite interactions in facilitating HT among animals3,7. Furthermore, the large amount of DNA generated by the amplification of the horizontally transferred transposons supports the idea that the exchange of genetic material between hosts and parasites influences their genomic evolution.