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Variation and constraints in hybrid genome formation

Abstract

Hybridization is an important source of variation; it transfers adaptive genetic variation across species boundaries and generates new species. Yet, the limits to viable hybrid genome formation are poorly understood. Here we investigated to what extent hybrid genomes are free to evolve by sequencing the genomes of four island populations of the homoploid hybrid Italian sparrow Passer italiae. We report that a variety of novel and fully functional hybrid genomic combinations are likely to have arisen independently on Crete, Corsica, Sicily and Malta, with differentiation in candidate genes for beak shape and plumage colour. However, certain genomic regions are invariably inherited from the same parent species, limiting variation. These regions are over-represented on the Z chromosome and harbour candidate incompatibility loci, including DNA-repair and mitonuclear genes. These gene classes may contribute to the general reduction of introgression on sex chromosomes. This study demonstrates that hybrid genomes may vary, and identifies new candidate reproductive isolation genes.

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Fig. 1: Population structuring of the focal taxa.
Fig. 2: Local adaptation, private variation and strong selection on the Z chromosome.
Fig. 3: Parental similarity across the Z chromosome.

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Acknowledgements

We thank M. Tesaker and BirdLife Malta for help with field work, L. Piñeiro and L. Bache-Mathiesen for providing morphological data, and A. Nilsson for comments on the manuscript. This work was funded by a Swedish Research Council post doctoral grant and a Wenner-Gren Fellowship to A.R. and a Norwegian Science Foundation grant to G-P.S. and A.R.

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A.R. conceived the study, carried out field work and laboratory work, designed analyses, analysed data and wrote the manuscript. C.N.T. helped design analyses, and provided scripts, F.E. carried out field work and the gene ontology analyses, J.S.H. carried out field work and the final touches in figure preparation, M.M. performed the BEAST and Saguaro analyses and M.R. performed the recombination rate analyses and principal component analysis. T.O.E. provided the house sparrow reference genome, and G.P.S. identified the study system, designed the sampling strategy and carried out field work. All co-authors commented on the manuscript.

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Correspondence to Anna Runemark.

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Runemark, A., Trier, C.N., Eroukhmanoff, F. et al. Variation and constraints in hybrid genome formation. Nat Ecol Evol 2, 549–556 (2018). https://doi.org/10.1038/s41559-017-0437-7

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