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Evidence that genetic drift not adaptation drives fast-Z and large-Z effects in 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. CEFE, University of Montpellier, CNRS, EPHE, IRD.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Laboratory of Biometry and Evolutionary Biology, University of Lyon 1, CNRS UMR 5558.
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The sex chromosomes have been hypothesized to play a key role in driving adaptation and speciation across many taxa. The reason for this is thought to be the hemizygosity of the heteromorphic part of sex chromosomes in the heterogametic sex, which exposes recessive mutations to natural and sexual selection. The exposure of recessive beneficial mutations increases their rate of fixation on the sex chromosomes, which results in a faster rate of evolution. In addition, genetic incompatibilities between sex-linked loci are exposed faster in the genomic background of hybrids of divergent species, which makes sex chromosomes contribute disproportionately to reproductive isolation. However, in birds, which show a Z/W sex determination system, the disproportionate role of the Z-chromosome in adaptation and reproductive isolation is still debated. Instead, genetic drift has been proposed as the main driver of the so-called fast-Z and large-Z effects in birds. Here, we address this question in Ficedula flycatchers based on population resequencing data of six flycatcher species. Our results provide evidence for both the fast-Z and large-Z effects in Ficedula flycatchers and that these two phenomena are driven by genetic drift rather than positive selection. Genomic scans of selective sweeps and fixed differences in fact suggest a reduced action of positive selection on the Z-chromosome. We propose that the observed reduction in the efficacy of purifying selection on the Z-chromosome helps to establish genetic incompatibilities between Z-linked and autosomal loci, which could result in pronounced selective sweep signatures for compensatory mutations on the autosomes.

Keywords [en]
speciation, reproductive isolation, sex chromosomes, gene flow, hybrid incompatibilities
National Category
Evolutionary Biology Genetics and Genomics
Identifiers
URN: urn:nbn:se:uu:diva-495932OAI: oai:DiVA.org:uu-495932DiVA, id: diva2:1734027
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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Chase, MadelineMugal, Carina

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