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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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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Author notes

  1. Phillip D. Zamore, Eric A. Miska, Peter Sarkies and Francis M. Jiggins contributed equally to this work.


  1. Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK

    • Samuel H. Lewis
    • , Melanie Tanguy
    • , Lise Frézal
    • , Eric A. Miska
    •  & Francis M. Jiggins
  2. Medical Research Council London Institute of Medical Sciences, Du Cane Road, London, W12 0NN, UK

    • Samuel H. Lewis
    •  & Peter Sarkies
  3. Institute for Clinical Sciences, Imperial College London, Du Cane Road, London, W12 0NN, UK

    • Samuel H. Lewis
    •  & Peter Sarkies
  4. Howard Hughes Medical Institute, RNA Therapeutics Institute, University of Massachusetts Medical School, 368 Plantation Street, Worcester, MA, 01605, USA

    • Kaycee A. Quarles
    • , Yujing Yang
    •  & Phillip D. Zamore
  5. Wellcome Trust/Cancer Research UK Gurdon Institute, Cambridge, CB2 1QN, UK

    • Melanie Tanguy
    • , Lise Frézal
    •  & Eric A. Miska
  6. Institut de Biologie de l’Ecole Normale Supérieure, Centre National de la Recherche Scientifique, Inserm, Ecole Normale Supérieure, Paris Sciences & Lettres Research University, 75005, Paris, France

    • Lise Frézal
  7. Department of Biomedical Sciences and Pathobiology, Virginia Maryland College of Veterinary Medicine, 205 Duck Pond Drive, Virginia Tech, Blacksburg, VA, 24061, USA

    • Stephen A. Smith
  8. Department of Zoology, University of Wisconsin–Madison, 352 Birge Hall, 430 Lincoln Drive, Madison, WI, 53706, USA

    • Prashant P. Sharma
  9. Université de Poitiers, Laboratoire Ecologie et Biologie des Interactions, Equipe Ecologie Evolution Symbiose, 5 Rue Albert Turpain, TSA 51106, 86073, Poitiers Cedex 9, France

    • Richard Cordaux
    • , Clément Gilbert
    •  & Isabelle Giraud
  10. Laboratoire Evolution, Génomes, Comportement, Écologie, Unité Mixte de Recherche 9191 Centre National de la Recherche Scientifique and Unité Mixte de Recherche 247 Institut de Recherche pour le Développement, Université Paris-Sud, 91198, Gif-sur-Yvette, France

    • Clément Gilbert
  11. School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, NR4 7TJ, UK

    • David H. Collins


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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.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

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

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