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A chromosome-level assembly of the Atlantic herring: detection of a supergene and other signals of selection
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, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.ORCID iD: 0000-0002-7570-6847
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, 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: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 29, no 11, p. 1919-1928Article in journal (Refereed) Published
Abstract [en]

The Atlantic herring is a model species for exploring the genetic basis for ecological adaptation, due to its huge population size and extremely low genetic differentiation at selectively neutral loci. However, such studies have so far been hampered because of a highly fragmented genome assembly. Here, we deliver a chromosome-level genome assembly based on a hybrid approach combining a de novo Pacific Biosciences (PacBio) assembly with Hi-C-supported scaffolding. The assembly comprises 26 autosomes with sizes ranging from 12.4 to 33.1 Mb and a total size, in chromosomes, of 726 Mb, which has been corroborated by a high-resolution linkage map. A comparison between the herring genome assembly with other high-quality assemblies from bony fishes revealed few inter-chromosomal but frequent intra-chromosomal rearrangements. The improved assembly facilitates analysis of previously intractable large-scale structural variation, allowing, for example, the detection of a 7.8-Mb inversion on Chromosome 12 underlying ecological adaptation. This supergene shows strong genetic differentiation between populations. The chromosome-based assembly also markedly improves the interpretation of previously detected signals of selection, allowing us to reveal hundreds of independent loci associated with ecological adaptation.

Place, publisher, year, edition, pages
Cold Spring Harbor Laboratory Press (CSHL), 2019. Vol. 29, no 11, p. 1919-1928
Keywords [en]
Atlantic herring, assembly, ecological adaptation, supergene
National Category
Genetics Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-396775DOI: 10.1101/gr.253435.119ISI: 000493952800015PubMedID: 31649060OAI: oai:DiVA.org:uu-396775DiVA, id: diva2:1368969
Funder
Knut and Alice Wallenberg FoundationSwedish Research CouncilThe Research Council of Norway, 254774Wellcome trust, WT108749/Z/15/ZAvailable from: 2019-11-09 Created: 2019-11-09 Last updated: 2019-11-28Bibliographically approved
In thesis
1. Genetic Adaptation and Speciation in Darwin’s Finches and Atlantic Herring
Open this publication in new window or tab >>Genetic Adaptation and Speciation in Darwin’s Finches and Atlantic Herring
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Natural selection acts on existing genetic variation to drive genetic adaptation of organisms to various ecological niches. Interaction between closely related populations, through processes such as competition and hybridization, may either lead to their divergence or population fusion, which has consequences for adaptation and the formation of species. This thesis aims to use two natural populations, Darwin’s finches and Atlantic herring, as models to explore the genetic mechanisms underlying ecological adaptation and speciation.

The ecological adaptation of Darwin’s finches across the Galápagos Islands is primarily reflected by variation in beak morphology. Using whole-genome re-sequencing of all Darwin’s finch species, we discover that a locus, HMGA2, is highly associated with variation in beak size. Data collected before and after a severe drought show that this locus plays a critical role for ecological character displacement in large ground finches Geospiza magnirostris and medium ground finches G. fortis.

Genomic islands of divergence refer to genomic regions of elevated divergence when comparing the genomes of closely related taxa. Establishment of these genomic islands can reflect a role in reproductive isolation or be related to ecological adaptation or background selection. Investigating their properties can shed light on how new species evolve. We study the landscape of genomic islands in Darwin’s finches, and find that the most pronounced genomic islands are likely ancient balanced polymorphisms, which govern adaptive variation in beak morphology.

Hybridization is increasingly recognized as an important evolutionary process which may lead to speciation. We study two cases of hybridization in Darwin’s finches. In the first case, a new lineage of Darwin’s finches was founded through hybridization between a resident medium ground finch G. fortis and an immigrant Española cactus finch G. conirostris. In the second case, female-biased introgression occurred predominantly from medium ground finches G. fortis to common cactus finches G. scandens. Our genetic analysis on the mosaic genomes of hybrid finches show that non-random mating and natural selection primarily determine the outcome of hybridization.

We generate a chromosome-level assembly of the Atlantic herring with a total size of 726 Mb, which coincides with a high-resolution linkage map and an LD-based recombination map. This facilitates the identification of an ~8Mb inversion, which is likely to be associated with ecological adaptation in herring to differences in water temperature. The contiguity of the assembly sorts placement of loci under selection that were identified based on a previous, highly fragmented draft assembly of the herring genome.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2020. p. 49
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Medicine, ISSN 1651-6206 ; 1620
Keywords
Darwin's finches, Atlantic herring, Population genetics, Evolution, Ecological adaptation, Speciation
National Category
Ecology Evolutionary Biology Genetics
Research subject
Biology with specialization in Animal Ecology; Bioinformatics
Identifiers
urn:nbn:se:uu:diva-397886 (URN)978-91-513-0826-5 (ISBN)
Public defence
2020-02-28, Room C8:305, BMC, Husargatan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2020-01-13 Created: 2019-11-28 Last updated: 2020-01-13

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Pettersson, MatsRochus, Christina MarieHan, FanHill, JasonWallerman, OlaBunikis, IgnasAndersson, Leif

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