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

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 17.

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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.).

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Affiliations

Authors

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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