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Biased Inference of Selection Due to GC-Biased Gene Conversion and the Rate of Protein Evolution in Flycatchers When Accounting for It
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Ludwig Maximilians Univ Munchen, Fac Biol, Dept Biol 2, Planegg Martinsried, Germany.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ Konstanz, Dept Biol, Chair Zool & Evolutionary Biol, Constance, Germany.
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2018 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 10, p. 2475-2486Article in journal (Refereed) Published
Abstract [en]

The rate of recombination impacts on rates of protein evolution for at least two reasons: it affects the efficacy of selection due to linkage and influences sequence evolution through the process of GC-biased gene conversion (gBGC). We studied how recombination, via gBGC, affects inferences of selection in gene sequences using comparative genomic and population genomic data from the collared flycatcher (Ficedula albicollis). We separately analyzed different mutation categories ("strong"-to-"weak" "weak-to-strong," and GC-conservative changes) and found that gBGC impacts on the distribution of fitness effects of new mutations, and leads to that the rate of adaptive evolution and the proportion of adaptive mutations among nonsynonymous substitutions are underestimated by 22-33%. It also biases inferences of demographic history based on the site frequency spectrum. In light of this impact, we suggest that inferences of selection (and demography) in lineages with pronounced gBGC should be based on GC-conservative changes only. Doing so, we estimate that 10% of nonsynonymous mutations are effectively neutral and that 27% of nonsynonymous substitutions have been fixed by positive selection in the flycatcher lineage. We also find that gene expression level, sex-bias in expression, and the number of protein-protein interactions, but not Hill-Robertson interference (HRI), are strong determinants of selective constraint and rate of adaptation of collared flycatcher genes. This study therefore illustrates the importance of disentangling the effects of different evolutionary forces and genetic factors in interpretation of sequence data, and from that infer the role of natural selection in DNA sequence evolution.

Place, publisher, year, edition, pages
OXFORD UNIV PRESS , 2018. Vol. 35, no 10, p. 2475-2486
Keywords [en]
d(N)/d(S), distribution of fitness effects, GC-biased gene conversion, gene expression, Hill-Robertson interference
National Category
Evolutionary Biology Genetics
Identifiers
URN: urn:nbn:se:uu:diva-372675DOI: 10.1093/molbev/msy149ISI: 000452566800011PubMedID: 30085180OAI: oai:DiVA.org:uu-372675DiVA, id: diva2:1277076
Available from: 2019-01-09 Created: 2019-01-09 Last updated: 2019-04-09Bibliographically approved
In thesis
1. Rates and patterns of molecular evolution in avian genomes
Open this publication in new window or tab >>Rates and patterns of molecular evolution in avian genomes
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Evolution is the change in inherited characteristics of a population through subsequent generations. The interplay of several evolutionary mechanisms determines the rate at which this change occurs. In short, genetic variation is generated though mutation, and the fate of these mutations in a population is determined mainly by the combined effect of genetic drift, natural selection and recombination. Elucidating the relative impact of these mechanisms is complex; making it a long-standing question in evolutionary biology. In this thesis, I focus on disentangling the relative roles of these evolutionary mechanisms and genetic factors in determining rates and patterns of evolution at the molecular level, by studying variation in the DNA sequence of multiple avian species, and in particular the collared flycatcher (Ficedula albicollis). Specifically, I aim to further our understanding regarding the impact of recombination rate on genome evolution, through its interaction with the efficacy of selection and through the process of GC-biased gene conversion (gBGC), which has been poorly characterized in birds. I demonstrate that gBGC has a pervasive effect on the genome of the collared flycatcher and other avian species, as it increases the substitution rate and affects interpretations of the impact of natural selection and adaptation. Interestingly, its effect is even stronger in neutrally evolving sites compared to sites evolving under selection. After accounting for gBGC, I disentangle the true impact of natural selection versus non-adaptive processes in determining rates of molecular evolution in the collared flycatcher genome, shedding light on the process of adaptation. Finally, I demonstrate the significant role of recombination through its impact on linked selection, along with mutation rate differences, in determining relative levels of genetic diversity and their relationship to the fast-Z effect across the avian phylogeny. This thesis urges future studies to account for the effect of recombination before interpreting patterns of selection in sequence evolution.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. p. 51
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1800
Keywords
Molecular evolution, recombination, GC-biased gene conversion, Hill-Robertson interference, effective population size, dN/dS, distribution of fitness effects, avian genomes, collared flycatcher, sex chromosomes
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-381373 (URN)978-91-513-0637-7 (ISBN)
Public defence
2019-06-11, Evolutionary Biology Center, Norbyvägen 14, Uppsala, 13:00 (English)
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Available from: 2019-05-20 Created: 2019-04-09 Last updated: 2019-06-17

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Bolivar, PaulinaMugal, CarinaSebastiano, Matteo RossiNater, AlexanderWang, MiDutoit, LudovicEllegren, Hans

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