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Epistatic mutations under divergent selection govern phenotypic variation in the crow hybrid zone

Nature Ecology & Evolution volume 3, pages 570–576 (2019)Cite this article

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Abstract

The evolution of genetic barriers opposing interspecific gene flow is key to the origin of new species. Drawing from information on over 400 admixed genomes sourced from replicate transects across the European hybrid zone between all-black carrion crows and grey-coated hooded crows, we decipher the interplay between phenotypic divergence and selection at the molecular level. Over 68% of plumage variation was explained by epistasis between the gene NDP and a ~2.8-megabase region on chromosome 18 with suppressed recombination. Both pigmentation loci showed evidence for divergent selection resisting introgression. This study reveals how few, large-effect loci can govern prezygotic isolation and shield phenotypic divergence from gene flow.

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Fig. 1: Genetic basis of phenotypic variation.
Fig. 2: Geographic and genomic cline analyses.

Data availability

Genotype and phenotype data are available in Supplementary Tables 1, 8, 10 and 11. R scripts used for the analyses are available as Supplementary Data 1–7.

References

  1. Wolf, J. B. W. & Ellegren, H. Nat. Rev. Genet. 18, 87–100 (2017).

    Article  CAS  PubMed  Google Scholar 

  2. Ravinet, M. et al. J. Evol. Biol. 30, 1450–1477 (2017).

    Article  CAS  PubMed  Google Scholar 

  3. Vijay, N. et al. Nat. Commun. 7, e13195 (2016).

    Article  Google Scholar 

  4. Mayr, E. Systematics and the Origin of Species (Columbia Univ. Press, 1942).

  5. Randler, C. Ardea 95, 143–149 (2007).

    Article  Google Scholar 

  6. Saino, N. & Scatizzi, L. Boll. Zool. 58, 255–260 (1991).

    Article  Google Scholar 

  7. Londei, T. Ibis 155, 632–634 (2013).

    Article  Google Scholar 

  8. Poelstra, J. W. et al. Science 344, 1410–1414 (2014).

    Article  CAS  PubMed  Google Scholar 

  9. Poelstra, J. W., Vijay, N., Hoeppner, M. P. & Wolf, J. B. W. Mol. Ecol. 24, 4617–4628 (2015).

    Article  CAS  PubMed  Google Scholar 

  10. Le Corre, V. & Kremer, A. Mol. Ecol. 21, 1548–1566 (2012).

    Article  PubMed  Google Scholar 

  11. Gompert, Z., Mandeville, E. G. & Buerkle, C. A. Annu. Rev. Ecol. Evol. Syst. 48, 207–229 (2017).

    Article  Google Scholar 

  12. Barton, N. H. & Hewitt, G. M. Annu. Rev. Ecol. Syst. 16, 113–148 (1985).

    Article  Google Scholar 

  13. Wu, C. C. et al. In situ quantification of individual mRNA transcripts in melanocytes discloses gene regulation of relevance to speciation. J. Exp. Biol. https://doi.org/10.1242/jeb.194431 (2019).

    Article  PubMed  Google Scholar 

  14. Ke, J. Y. et al. Gene Dev. 27, 2305–2319 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Vickrey, A. I. et al. eLife 7, e34803 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  16. Haas, F. et al. Mol. Ecol. 18, 294–305 (2009).

    Article  CAS  PubMed  Google Scholar 

  17. Szymura, J. M. & Barton, N. H. Evolution 40, 1141–1159 (1986).

    PubMed  Google Scholar 

  18. Weissensteiner, M. H. et al. Genome Res. 27, 697–708 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kofron, M. et al. Dev. Biol. 237, 183–201 (2001).

    Article  CAS  PubMed  Google Scholar 

  20. Duquet, M. Ornithos 19, 57–67 (2012).

    Google Scholar 

  21. Rolando, A. Ornis Scand. 24, 80–83 (1993).

    Article  Google Scholar 

  22. Mackay, T. F. C. Nat. Rev. Genet. 15, 22–33 (2014).

    Article  CAS  PubMed  Google Scholar 

  23. Pennisi, E. Science 345, 611–613 (2014).

    Article  CAS  PubMed  Google Scholar 

  24. Nadeau, N. J. et al. Genome Res. 24, 1316–1333 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Toews, D. P. L. et al. Curr. Biol. 26, 2313–2318 (2016).

    Article  CAS  PubMed  Google Scholar 

  26. Brodin, A. & Haas, F. Anim. Behav. 72, 139–146 (2006).

    Article  Google Scholar 

  27. Brodin, A. & Haas, F. Evol. Ecol. 23, 17–29 (2009).

    Article  Google Scholar 

  28. Saino, N. & Villa, S. Auk 109, 543–555 (1992).

    Google Scholar 

  29. Seehausen, O. et al. Nature 455, 620–626 (2008).

    Article  CAS  PubMed  Google Scholar 

  30. Coyne, J. A. & Orr, H. A. Evolution 51, 295–303 (1997).

    Article  PubMed  Google Scholar 

  31. Untergasser, A. et al. Nucleic Acids Res. 40, e115 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. DePristo, M. A. et al. Nat. Genet. 43, 491–498 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Gompert, Z. & Buerkle, C. A. Mol. Ecol. Resour. 10, 378–384 (2010).

    Article  CAS  PubMed  Google Scholar 

  34. R Development Core Team R: a Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  35. Anderson, E. C. & Thompson, E. A. Genetics 160, 1217–1229 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Wringe, B. F., Stanley, R. R. E., Jeffery, N. W., Anderson, E. C. & Bradbury, I. R. Mol. Ecol. Resour. 17, 91–95 (2017).

    Article  CAS  PubMed  Google Scholar 

  37. Vähä, J. P. & Primmer, C. R. Mol. Ecol. 15, 63–72 (2006).

    Article  PubMed  Google Scholar 

  38. Wringe, B. F., Stanley, R. R. E., Jeffery, N. W., Anderson, E. C. & Bradbury, I. R. Mol. Ecol. Resour. 17, e275–e284 (2017).

    Article  CAS  PubMed  Google Scholar 

  39. Nielsen, E. E., Bach, L. A. & Kotlicki, P. Mol. Ecol. Notes 6, 971–973 (2006).

    Article  Google Scholar 

  40. Josse, J. & Husson, F. J. Stat. Softw. 70, 1–31 (2016).

    Article  Google Scholar 

  41. Lê, S., Josse, J. & Husson, F. J. Stat. Softw. 25, 1–18 (2008).

    Article  Google Scholar 

  42. Stoffel, M. A., Nakagawa, S. & Schielzeth, H. Methods Ecol. Evol. 8, 1639–1644 (2017).

    Article  Google Scholar 

  43. Aulchenko, Y. S., Ripke, S., Isaacs, A. & Van Duijn, C. M. Bioinformatics 23, 1294–1296 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. Gao, X. Y., Stamier, J. & Martin, E. R. Genet. Epidemiol. 32, 361–369 (2008).

    Article  PubMed  Google Scholar 

  45. Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference 2nd edn (Springer, 1998).

  46. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer, 1998).

  47. Derryberry, E. P., Derryberry, G. E., Maley, J. M. & Brumfield, R. T. Mol. Ecol. Resour. 14, 652–663 (2014).

    Article  PubMed  Google Scholar 

  48. Szymura, J. M. & Barton, N. H. Evolution 45, 237–261 (1991).

    PubMed  Google Scholar 

  49. Metropolis, N., Rosenbluth, A. W., Rosenbluth, M. N., Teller, A. H. & Teller, E. J. Chem. Phys. 21, 1087–1092 (1953).

    Article  CAS  Google Scholar 

  50. Hastings, W. K. Biometrika 57, 97–109 (1970).

    Article  Google Scholar 

  51. Bailey, R. gghybrid: Evolutionary analysis of hybrids and hybrid zones. R package version 0.0.0.9000 (2018).

  52. Gompert, Z. & Buerkle, C. A. Mol. Ecol. Resour. 12, 1168–1176 (2012).

    Article  CAS  PubMed  Google Scholar 

  53. Buerkle, C. A. Mol. Ecol. Notes 5, 684–687 (2005).

    Article  CAS  Google Scholar 

  54. Fitzpatrick, B. M. Ecol. Evol. 3, 1951–1966 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Sung, C. J., Bell, K. L., Nice, C. C. & Martin, N. H. Mol. Ecol. 27, 959–978 (2018).

    Article  CAS  PubMed  Google Scholar 

  56. Purcell, S. et al. Am. J. Hum. Genet. 81, 559–575 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Goude, J. & Jombart, T. hierfstat: Estimation and tests of hierarchical F-statistics. R package version 0.04-22 (2015).

  58. Ma, J. Z. & Amos, C. I. PLoS ONE 7, e40224 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Knief, U. et al. Genome Biol. 17, e199 (2016).

    Article  Google Scholar 

  60. Duforet-Frebourg, N., Luu, K., Laval, G., Bazin, E. & Blum, M. G. B. Mol. Biol. Evol. 33, 1082–1093 (2016).

    Article  CAS  PubMed  Google Scholar 

  61. Zheng, X. W. et al. Bioinformatics 28, 3326–3328 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study would not have been possible without the commitment of dedicated ornithologists who helped to locate active nest sites and participated in sampling. These include M. Hug and colleagues in Brandenburg, J. Voigt, D. Kronbach, J. Wollmerstädt, M. Schrack and W. Nachtigall in Sachsen, M. Döpfner in Baden-Württemberg, S. Zinko and M. Grossmann in Austria, and personnel of the Amministrazione Provinciale of Alessandria, Asti and Cuneo in Italy. We further acknowledge the Max Planck Institute for Ornithology in Radolfzell, the Friedrich-Löffler-Institute and the Förderverein Sächsische Vogelschutzwarte Neschwitz e. V. for help with the organization of field work. The UPPMAX Next-Generation Sequencing Cluster and Storage (UPPNEX) project, funded by the Knut and Alice Wallenberg Foundation and Swedish National Infrastructure for Computing, provided access to computational resources. Funding was provided by the VolkswagenStiftung (grant I/83 496 to J.B.W.W.), European Research Council (ERCStG-336536 FuncSpecGen to J.B.W.W.), Knut and Alice Wallenberg Foundation (project grant including J.B.W.W.) and LMU Munich (to J.B.W.W.).

Author information

Author notes

  1. These authors contributed equally: Ulrich Knief, Christen M. Bossu.

Authors and Affiliations

  1. Division of Evolutionary Biology, Faculty of Biology, LMU Munich, Munich, Germany

    Ulrich Knief, Matthias Weissensteiner & Jochen B. W. Wolf

  2. Science for Life Laboratories and Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden

    Christen M. Bossu, Jelmer Poelstra, Nagarjun Vijay, Matthias Weissensteiner & Jochen B. W. Wolf

  3. Population Genetics, Department of Zoology, Stockholm University, Stockholm, Sweden

    Christen M. Bossu

  4. Institute of the Environment and Sustainability, Center for Tropical Research, University of California, Los Angeles, CA, USA

    Christen M. Bossu

  5. Department of Environmental Science and Policy, University of Milan, Milan, Italy

    Nicola Saino

  6. Department of Biology, Lund University, Lund, Sweden

    Bengt Hansson

  7. Biology Department, Duke University, Durham, NC, USA

    Jelmer Poelstra

  8. Department of Biological Sciences, Indian Institute of Science Education and Research, Bhopal, India

    Nagarjun Vijay

Authors
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Contributions

U.K., C.M.B. and J.B.W.W. conceived of the study design. C.M.B., J.P., M.W., B.H., N.S. and J.B.W.W. conducted the field work and provided samples. C.M.B. and U.K. performed all analyses. N.S. and J.P. helped with phenotype scoring, and N.V. assisted in SNP design. U.K., C.M.B. and J.B.W.W. wrote the manuscript with input from all other authors.

Corresponding author

Correspondence to Jochen B. W. Wolf.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary Text, Supplementary Figures 1–15 and Supplementary Tables 2–7, 9, 12 and 13

Reporting Summary

Supplementary Table 1

List of SNP markers genotyped with the GoldenGate Assay (Illumina), their genomic location (genome version 2.5) and associated primer sequences.

Supplementary Table 8

Genotype and additional sampling data on all individuals (both GoldenGate Assay genotyping and GATK genotyping).

Supplementary Table 10

Phenotypic information on all individuals.

Supplementary Table 11

Information on the ancestral state of all SNPs.

Supplementary Code 1

Perform PCA on phenotypic data.

Supplementary Code 2

Prepare genotype data for NewHybrids and execute NewHybrids through R.

Supplementary Code 3

Estimate FIS and confidence intervals.

Supplementary Code 4

Convert genotype data to PLINK format, estimate FST and perform PCA on genotypes.

Supplementary Code 5

Estimate hybrid indices and fit geographic clines.

Supplementary Code 6

Estimate hybrid indices on subsets of SNPs and fit genomic clines.

Supplementary Code 7

Perform genome-wide association study and fit linear models with interactions between specific SNPs.

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Knief, U., Bossu, C.M., Saino, N. et al. Epistatic mutations under divergent selection govern phenotypic variation in the crow hybrid zone. Nat Ecol Evol 3, 570–576 (2019). https://doi.org/10.1038/s41559-019-0847-9

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