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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.

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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.

Change history

  • 08 May 2025

    In the version of this article initially published, the Supplementary Table and Code files were mislinked and are now amended in the HTML version of the article.

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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 Code

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

Supplementary Code

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

Supplementary Code

Phenotypic information on all individuals.

Supplementary Code

Information on the ancestral state of all SNPs.

Supplementary Code

Perform PCA on phenotypic data.

Supplementary Code

Prepare genotype data for NewHybrids and execute NewHybrids through R.

Supplementary Code

Estimate FIS and confidence intervals.

Supplementary Table

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

Supplementary Table

Estimate hybrid indices and fit geographic clines.

Supplementary Table

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

Supplementary Table 11

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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