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The combination of HiFi and HiC sequencing technologies enables the investigation of structural variants in speciation of Ficedula flycatchers
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0002-7916-3560
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University, Disciplinary Domain of Science and Technology, Mathematics and Computer Science, Department of Information Technology.ORCID iD: 0000-0001-5235-6461
Stockholm University, Department of Zoology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0002-9885-1537
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Structural variants, typically defined as mutations affecting more than 50bp, have been shown to encompass a significant portion of the genome and can have large phenotypic effects. Additionally, increasing empirical evidence demonstrates that structural variants may play a substantial role in speciation, which could previously have been overlooked because of difficulties in identifying them with short-read data. However, with the increased availability of long-read sequencing technology we are now equipped better than ever to address this limitation and study the contribution of different types of structural variants to genetic variation within and genetic differentiation between closely related species. Here, we follow this approach and combine PacBio HiFi and HiC sequencing for two closely related passerine birds, the collared flycatcher and the pied flycatcher. This enables us to generate a chromosome-level genome assembly for both species, and identify structural variants between the two species. Based on population-level HiFi sequencing for both species, we then investigate patterns of single nucleotide diversity and differentiation within and between species and their association with different types of structural variation. We find widespread structural variation between the two species, where both the sex chromosomes show a disproportionate number of structural variants, which may help explain the suspected role of the Z-chromosome in contributing to genetic incompatibilities. We also find that genomic differentiation peaks are enriched in both translocations and inversions, which supports a mechanistic role of structural variation in population differentiation and speciation.

Keywords [en]
speciation genomics, long-read genome assembly, avian microchromosomes, chromosomal re-arrangements, inversions
National Category
Genetics and Genomics Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-495935OAI: oai:DiVA.org:uu-495935DiVA, id: diva2:1734031
Funder
Swedish Research Council, 2013-8271Swedish Research Council, 2016-05138Knut and Alice Wallenberg Foundation, 2014/0044Swedish Research Council, 2019-03952EU, European Research Council, No.851753Available from: 2023-02-04 Created: 2023-02-04 Last updated: 2025-02-01
In thesis
1. Speciation genomics in Ficedula flycatchers
Open this publication in new window or tab >>Speciation genomics in Ficedula flycatchers
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Understanding what evolutionary processes have shaped patterns of genomic differentiation between species is a major aim of speciation genomics. However, disentangling the role of different processes that generate similar patterns remains a substantial challenge. Within this thesis, I aimed to infer the action of different evolutionary processes through population-level genome re-sequencing of closely related species. I explored how processes such as recombination, natural selection, and genetic drift interact to shape the genomic differentiation landscape among multiple species of Ficedula flycatcher. Collared flycatcher and pied flycatcher are a pair of closely related species, which hybridize in regions of secondary contact. Reproductive isolation is strong and hybrids appear to be sterile. I compared the differentiation landscape between collared and pied flycatchers with a more distantly related species pair, the red-breasted and taiga flycatchers. This comparison revealed elevated regions of genomic differentiation shared between the two pairs, i.e. shared differentiation peaks, and those unique to a single pair, i.e. lineage-specific differentiation peaks. Since the two species pairs share a negligible portion of genetic variation, shared patterns in the differentiation landscape should be driven and maintained by conserved processes, while lineage-specific patterns should be driven by lineage-specific changes in relevant evolutionary processes. Selective sweep scans suggested that both shared and lineage-specific peaks can result from adaptive evolution and that lineage-specific adaptation is not a sufficient determinant of lineage-specific peaks. Instead, lineage-specific differentiation peaks appeared to be driven by evolutionary changes in the recombination landscape, the dynamics of which had strong impacts on the detection of signatures of linked selection. I also found that adaptation did not play a prominent role on Z-chromosome differentiation. Both the fast-Z and large-Z effects were apparent within the flycatchers but appeared to be primarily driven by the increased role of genetic drift on the Z-chromosome due to its reduced effective population size compared to the autosomes. I hypothesized that the increased impact of genetic drift could speed up the buildup of genetic incompatibilities of Z-linked and autosomal loci and contribute to reproductive isolation. Finally, using long-read and HiC sequencing data, I generated high-quality reference genomes for the collared flycatcher and pied flycatcher, and provided a first glimpse of the role of structural variation in speciation. I observed an increased prevalence of inversions and translocations on the sex chromosomes and in differentiation peaks. Structural rearrangements may therefore represent an important source of genomic variation contributing to species divergence.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2023. p. 71
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2239
Keywords
recombination, linked selection, selective sweeps, sex chromosomes, structural variation, birds, genome assembly
National Category
Evolutionary Biology Genetics and Genomics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-495937 (URN)978-91-513-1711-3 (ISBN)
Public defence
2023-03-24, Lindahlsalen, Evolutionary Biology Center, Norbyvägen 18A, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2023-03-02 Created: 2023-02-04 Last updated: 2025-02-01

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Chase, MadelineScofield, DouglasSegami, CarolinaÅlund, MurielleQvarnström, AnnaMugal, Carina

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