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Chromosomal inversions associated with environmental adaptation in honeybees
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala University, Science for Life Laboratory, SciLifeLab.ORCID iD: 0000-0002-6355-7581
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala University, Science for Life Laboratory, SciLifeLab.
Uppsala University, Science for Life Laboratory, SciLifeLab. Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology.
Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala University, Science for Life Laboratory, SciLifeLab.
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2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 6, p. 1358-1374Article in journal (Refereed) Published
Abstract [en]

Chromosomal inversions can facilitate local adaptation in the presence of gene flow by suppressing recombination between well-adapted native haplotypes and poorly adapted migrant haplotypes. East African mountain populations of the honeybee Apis mellifera are highly divergent from neighbouring lowland populations at two extended regions in the genome, despite high similarity in the rest of the genome, suggesting that these genomic regions harbour inversions governing local adaptation. Here, we utilize a new highly contiguous assembly of the honeybee genome to characterize these regions. Using whole-genome sequencing data from 55 highland and lowland bees, we find that the highland haplotypes at both regions are present at high frequencies in three independent highland populations but extremely rare elsewhere. The boundaries of both divergent regions are characterized by regions of high homology with each other positioned in opposite orientations and contain highly repetitive, long inverted repeats with homology to transposable elements. These regions are likely to represent inversion breakpoints that participate in nonallelic homologous recombination. Using long-read data, we confirm that the lowland samples are contiguous across breakpoint regions. We do not find evidence for disruption of functional sequence by these breakpoints, which suggests that the inversions are likely maintained due to their allelic content conferring local adaptation in highland environments. Finally, we identify a third divergent genomic region, which contains highly divergent segregating haplotypes that also may contain inversion variants under selection. The results add to a growing body of evidence indicating the importance of chromosomal inversions in local adaptation.

Place, publisher, year, edition, pages
WILEY , 2019. Vol. 28, no 6, p. 1358-1374
Keywords [en]
chromosomal inversion, honeybee, local adaptation, long-read sequencing, nonallelic homologous recombination, structural variation
National Category
Genetics
Identifiers
URN: urn:nbn:se:uu:diva-383207DOI: 10.1111/mec.14944ISI: 000465219200012PubMedID: 30431193OAI: oai:DiVA.org:uu-383207DiVA, id: diva2:1317587
Funder
Swedish Research Council Formas, 2013-722Swedish Research Council, 2014-5096Available from: 2019-05-23 Created: 2019-05-23 Last updated: 2019-08-12Bibliographically approved

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Christmas, Matthew JWallberg, AndreasBunikis, IgnasOlsson, AnnaWallerman, OlaWebster, Matthew T

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Christmas, Matthew JWallberg, AndreasBunikis, IgnasOlsson, AnnaWallerman, OlaWebster, Matthew T
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Department of Medical Biochemistry and MicrobiologyScience for Life Laboratory, SciLifeLabDepartment of Immunology, Genetics and Pathology
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