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Transitions between phases of genomic differentiation during stick-insect speciation

Nature Ecology & Evolution volume 1, Article number: 0082 (2017) Cite this article

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Abstract

Speciation can involve a transition from a few genetic loci that are resistant to gene flow to genome-wide differentiation. However, only limited data exist concerning this transition and the factors promoting it. Here, we study phases of speciation using data from >100 populations of 11 species of Timema stick insects. Consistent with early phases of genic speciation, adaptive colour-pattern loci reside in localized genetic regions of accentuated differentiation between populations experiencing gene flow. Transitions to genome-wide differentiation are also observed with gene flow, in association with differentiation in polygenic chemical traits affecting mate choice. Thus, intermediate phases of speciation are associated with genome-wide differentiation and mate choice, but not growth of a few genomic islands. We also find a gap in genomic differentiation between sympatric taxa that still exchange genes and those that do not, highlighting the association between differentiation and complete reproductive isolation. Our results suggest that substantial progress towards speciation may involve the alignment of multi-faceted aspects of differentiation.

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Figure 1: Conceptual overview and summary of genomic differentiation in Timema .
Figure 2: Localized genetic differentiation ( FST) in T. cristinae .
Figure 3: CHCs and genome-wide differentiation in T. cristinae .
Figure 4: Whole-genome analyses of genomic differentiation ( FST) in Timema .
Figure 5: A gap in genomic differentiation (mean genome-wide F ST ) for Timema taxa in sympatry.
Figure 6: Temporal dynamics of the evolution of sexual isolation and morphological differentiation.

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Acknowledgements

We thank R. Guillem, R. Kather, J. Stapley and T. Schwander for their advice; the Oakley-, Kuris- and Lafferty-groups at University of California Santa Barbara for their support; L. Jeanson and J. Hosegood for the phenotypic measurements and lab work; R. Marin for drawing all the figures; T. Schwander for providing the genetic crosses used for linkage mapping; the High-Throughput Genomics Group at the Wellcome Trust Centre for Human Genetics (funded by Wellcome Trust grant reference 090532/Z/09/Z and MRC Hub grant G0900747 91070) for generating the whole-genome re-sequencing data; and the National Center for Genome Sequencing (USA) for the GBS data. R.R. was supported by the Human Frontier Science Program, M.M. and K.L. were supported by the Swiss National Science Foundation and P.N. was supported by the Royal Society of London. The work was funded by grants from the European Research Council (grant NatHisGen R/129639 to P.N.) and the Natural Science and Engineering Research Council of Canada (to B.J.C. and G.G.). Computing, storage and other resources from the Division of Research Computing in the Office of Research and Graduate Studies at Utah State University, as well as access to the High Performance Computing Facilities, particularly to the Iceberg HPC cluster, from the Corporate Information and Computing Services at the University of Sheffield, are gratefully acknowledged.

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  1. Rüdiger Riesch, Moritz Muschick, Dorothea Lindtke, Romain Villoutreix and Zach Gompert: These authors contributed equally to this work.

Authors and Affiliations

  1. School of Biological Sciences, Royal Holloway, University of London, Egham, TW20 0EX, Surrey , UK

    Rüdiger Riesch

  2. Aquatic Ecology & Evolution, Institute of Ecology and Evolution, CH-3012, Bern, University of Bern, Switzerland

    Moritz Muschick

  3. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, South Yorkshire S10 2TN, UK

    Dorothea Lindtke, Romain Villoutreix, Kay Lucek, Elizabeth Hellen, Víctor Soria-Carrasco, Clarissa F. de Carvalho & Patrik Nosil

  4. Department of Biology, University of North Carolina, Chapel Hill, 27599, North Carolina, USA

    Aaron A. Comeault

  5. Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, 06369, Connecticut, USA

    Timothy E. Farkas

  6. Department of Aquatic Ecology, Eawag Swiss Federal Institute of Aquatic Science and Technology, Überlandstrasse 133, Dübendorf, Zurich, 8600, Switzerland

    Stuart R. Dennis

  7. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, 80309, Colorado, USA

    Rebecca J. Safran

  8. Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, 93106, California, USA

    Cristina P. Sandoval

  9. Department of Biology, Notre Dame University, South Bend, 11111, Indiana, USA

    Jeff Feder

  10. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada

    Regine Gries, Bernard J. Crespi & Gerhard Gries

  11. Department of Biology, Utah State University, Logan, 84322, Utah, USA

    Zach Gompert

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Contributions

R.R., Z.G., M.M., G.G., J.F., B.J.C. and P.N. conceived the project. R.R., R.V., D.L., M.M., A.A.C., R.G., T.E.F., C.P.S., C.F.d.C. and P.N. collected the data. R.R., D.L., M.M., R.V., Z.G. and P.N. led the data analyses, aided by V.S.-C., K.L., C.F.d.C. and S.R.D. R.R., Z.G. and P.N. wrote the initial manuscript and all authors contributed to further writing and revisions. Z.G. and V.S.-C. organized the data archiving. R.R., M.M., D.L., R.V. and Z.G. contributed equally.

Corresponding authors

Correspondence to Rüdiger Riesch, Zach Gompert or Patrik Nosil.

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Supplementary Methods; Supplementary Tables 1–15; Supplementary Figures 1–4 (PDF 3977 kb)

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Riesch, R., Muschick, M., Lindtke, D. et al. Transitions between phases of genomic differentiation during stick-insect speciation. Nat Ecol Evol 1, 0082 (2017). https://doi.org/10.1038/s41559-017-0082

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