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Recombination suppression and selection affect local ancestries in genomes of a migratory songbird

Jun Ishigohoka, Karen Bascón-Cardozo, Andrea Bours, Janina Fuß, Arang Rhie, Jacquelyn Mountcastle, Bettina Haase, William Chow, Joanna Collins, Kerstin Howe, Marcela Uliano-Silva, View ORCID ProfileOlivier Fedrigo, Erich D. Jarvis, Javier Pérez-Tris, Juan Carlos Illera, View ORCID ProfileMiriam Liedvogel
doi: https://doi.org/10.1101/2021.12.22.473882
Jun Ishigohoka
1Max Planck Institute for Evolutionary Biology, Plön, Germany
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Karen Bascón-Cardozo
1Max Planck Institute for Evolutionary Biology, Plön, Germany
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Andrea Bours
1Max Planck Institute for Evolutionary Biology, Plön, Germany
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Janina Fuß
2Institute of Clinical Molecular Biology (IKMB), Kiel University, Kiel, Germany
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Arang Rhie
3Genome Informatics Section, Computational and Statistical Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, USA
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Jacquelyn Mountcastle
4The Vertebrate Genome Lab, Rockefeller University, New York, NY, USA
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Bettina Haase
4The Vertebrate Genome Lab, Rockefeller University, New York, NY, USA
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William Chow
5Wellcome Sanger Institute, Cambridge, UK
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Joanna Collins
5Wellcome Sanger Institute, Cambridge, UK
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Kerstin Howe
5Wellcome Sanger Institute, Cambridge, UK
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Marcela Uliano-Silva
5Wellcome Sanger Institute, Cambridge, UK
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Olivier Fedrigo
4The Vertebrate Genome Lab, Rockefeller University, New York, NY, USA
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  • ORCID record for Olivier Fedrigo
Erich D. Jarvis
4The Vertebrate Genome Lab, Rockefeller University, New York, NY, USA
6Laboratory of Neurogenetics of Language, Rockefeller University, New York, NY, USA
7The Howards Hughes Medical Institute, Chevy Chase, MD, USA
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Javier Pérez-Tris
8Department of Biodiversity, Ecology and Evolution, Complutense University of Madrid, Madrid, Spain
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Juan Carlos Illera
9Biodiversity Research Institute (CSIC-Oviedo University-Principality of Asturias), Oviedo University, Mieres, Spain
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Miriam Liedvogel
1Max Planck Institute for Evolutionary Biology, Plön, Germany
10Institute of Avian Research, Wilhelmshaven, Germany
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  • ORCID record for Miriam Liedvogel
  • For correspondence: miriam.liedvogel@ifv-vogelwarte.de
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Abstract

The patterns of genetic relatedness among individuals vary along the genome, representing fluctuation of local ancestry. The factors responsible for this variation have not been well studied in wild animals with ecological and behavioural relevance. Here, we characterise the genomic architecture of genetic relatedness in the Eurasian blackcap, an iconic songbird species in ecology and quantitative genetics of migratory behaviour. We identify 23 genomic regions with deviated local relatedness patterns, using a chromosome-level de novo assembly of the blackcap genome and whole-genome resequencing data of 179 individuals from nine populations with diverse migratory phenotypes. Five genomic regions show local relatedness patterns of polymorphic inversions, three of which are syntenic to polymorphic inversions known in the zebra finch. Phylogenetic analysis reveals these three polymorphic inversions evolved independently in the blackcap and zebra finch indicating convergence of polymorphic inversions. Population genetic analyses in these three inversions in the blackcap suggest balancing selection between two haplotypes in one locus and background selection in the other two loci. One genomic region with deviated local relatedness is under selection against gene flow by population-specific reduction in recombination rate. Other genomic islands including 11 pericentromeric regions consist of evolutionarily conserved and non-conserved recombination cold-spots under background selection. Two of these regions with non-conserved recombination suppression are known to be associated with population-specific migratory phenotypes, where local relatedness patterns support additional effects of population-specific selection. These results highlight how different forms of recombination suppression and selection jointly affect heterogeneous genomic landscape of local ancestries.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 23, 2021.
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Recombination suppression and selection affect local ancestries in genomes of a migratory songbird
Jun Ishigohoka, Karen Bascón-Cardozo, Andrea Bours, Janina Fuß, Arang Rhie, Jacquelyn Mountcastle, Bettina Haase, William Chow, Joanna Collins, Kerstin Howe, Marcela Uliano-Silva, Olivier Fedrigo, Erich D. Jarvis, Javier Pérez-Tris, Juan Carlos Illera, Miriam Liedvogel
bioRxiv 2021.12.22.473882; doi: https://doi.org/10.1101/2021.12.22.473882
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Recombination suppression and selection affect local ancestries in genomes of a migratory songbird
Jun Ishigohoka, Karen Bascón-Cardozo, Andrea Bours, Janina Fuß, Arang Rhie, Jacquelyn Mountcastle, Bettina Haase, William Chow, Joanna Collins, Kerstin Howe, Marcela Uliano-Silva, Olivier Fedrigo, Erich D. Jarvis, Javier Pérez-Tris, Juan Carlos Illera, Miriam Liedvogel
bioRxiv 2021.12.22.473882; doi: https://doi.org/10.1101/2021.12.22.473882

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