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The role of recombination dynamics in shaping signatures of direct and indirect selection across the Ficedula flycatcher genome
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.
(English)In: Article in journal (Other academic) Submitted
Abstract [en]

Recombination is a central evolutionary process that reshuffles combinations of alleles along chromosomes, and consequently is expected to influence the efficacy of direct selection via Hill-Robertson interference. Additionally, the indirect effects of selection on neutral genetic diversity are expected to show a negative relationship with recombination rate, as background selection and genetic hitchhiking are stronger when recombination rate is low. However, owing to the limited availability of recombination rate estimates across divergent species, less is known about the impact of evolutionary changes in recombination rate on genomic signatures of selection. To address this question, we estimate recombination rate in two Ficedula flycatcher species, the taiga flycatcher (F. albicilla) and collared flycatcher (F. albicollis). We show that recombination rate is strongly correlated with signatures of indirect selection, and that evolutionary changes in recombination rate between species have observable impacts on this relationship. Conversely, signatures of direct selection on coding sequences show little to no relationship with recombination rate, even when restricted to genes where recombination rate is conserved between species. Thus, using measures of indirect and direct selection that bridge micro- and macro-evolutionary timescales, we demonstrate that the role of recombination rate and its dynamics varies for different signatures of selection.

Keywords [en]
meiotic recombination, linked selection, direct selection, speciation, Hill-Robertson interference
National Category
Evolutionary Biology Genetics and Genomics
Identifiers
URN: urn:nbn:se:uu:diva-495934DOI: 10.1101/2022.08.11.503468OAI: oai:DiVA.org:uu-495934DiVA, id: diva2:1734030
Funder
Knut and Alice Wallenberg Foundation, 2014/0044Swedish Research Council, 2013-8271Available 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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