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Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements

Abstract

In animals, small RNA molecules termed PIWI-interacting RNAs (piRNAs) silence transposable elements (TEs), protecting the germline from genomic instability and mutation. piRNAs have been detected in the soma in a few animals, but these are believed to be specific adaptations of individual species. Here, we report that somatic piRNAs were probably present in the ancestral arthropod more than 500 million years ago. Analysis of 20 species across the arthropod phylum suggests that somatic piRNAs targeting TEs and messenger RNAs are common among arthropods. The presence of an RNA-dependent RNA polymerase in chelicerates (horseshoe crabs, spiders and scorpions) suggests that arthropods originally used a plant-like RNA interference mechanism to silence TEs. Our results call into question the view that the ancestral role of the piRNA pathway was to protect the germline and demonstrate that small RNA silencing pathways have been repurposed for both somatic and germline functions throughout arthropod evolution.

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Fig. 1: Genes in small RNA pathways evolve rapidly throughout the arthropods.
Fig. 2: piRNAs are absent in the B. terrestris male germline.
Fig. 3: Somatic piRNAs are widespread and target TEs throughout the arthropods.
Fig. 4: Virally derived small RNAs in three arthropod species.
Fig. 5: A model of the divergent small RNA pathways silencing TEs in different arthropods.

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Acknowledgements

We thank A. McGregor, D. Leite, M. Akam, R. Jenner, R. Kilner, A. Duarte, C. Jiggins, R. Wallbank, A. Bourke, T. Dalmay, N. Moran, K. Warchol, R. Callahan, G. Farley and T. Livdahl for providing the arthropods. H. Robertson provided the D. virgifera genome sequence. This research was supported by a Leverhulme Research Project Grant (RPG-2016-210 to F.M.J., E.A.M. and P.S.), a European Research Council grant (281668 DrosophilaInfection to F.M.J.), a Medical Research Council grant (MRC MC-A652-5PZ80 to P.S.), an Imperial College Research Fellowship (to P.S.), Cancer Research UK (C13474/A18583 and C6946/A14492 to E.A.M.), the Wellcome Trust (104640/Z/14/Z and 092096/Z/10/Z to E.A.M.) and a National Institutes of Health R37 grant (GM62862 to P.D.Z.).

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S.H.L. and K.A.Q. performed the experiments with assistance from Y.Y., M.T., L.F., S.A.S., P.P.S., R.C., C.G., I.G. and D.H.C. S.H.L., K.A.Q. and P.S. carried out the computational analysis. P.D.Z., E.A.M., P.S. and F.M.J. supervised the project. S.H.L., K.A.Q., P.D.Z., E.A.M., P.S. and F.M.J. wrote the paper.

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Correspondence to Samuel H. Lewis or Francis M. Jiggins.

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Lewis, S.H., Quarles, K.A., Yang, Y. et al. Pan-arthropod analysis reveals somatic piRNAs as an ancestral defence against transposable elements. Nat Ecol Evol 2, 174–181 (2018). https://doi.org/10.1038/s41559-017-0403-4

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