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

Abstract

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.

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Figure 1: Taxonomic distribution and age of SPIN, OC1, ET and hAT1.
Figure 2: Biogeographic and phylogenetic evidence supporting horizontal transfers of SPIN and OC1 transposons on multiple continents.

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Acknowledgements

We thank E. Betrán, J. Demuth, T. Fondon, B. Koskella, J. Meik, E. Pritham, Q. Wang and members of the Feschotte laboratory for comments and suggestions during the preparation of the manuscript; M. Batzer, E. Dotson, S. Goodman, A. Prelat, T. Robinson, A. Ropiquet and the Grosell and Sánchez laboratories for the gifts of tissue samples used in this study; and J. Spieth and The Genome Center at Washington University School of Medicine in St Louis for permission to use the R. prolixus assembly before publication. C.F. is funded by the National Institutes of Health and S.S. by the National Science Foundation.

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C.G., S.S. and C.F. designed research, performed research, and analysed data. J.K.P. contributed data and perl scripts. P.J.B. contributed reagents and materials. C.G., S.S. and C.F. wrote the paper.

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Correspondence to Cédric Feschotte.

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Gilbert, C., Schaack, S., Pace II, J. et al. A role for host–parasite interactions in the horizontal transfer of transposons across phyla. Nature 464, 1347–1350 (2010). https://doi.org/10.1038/nature08939

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