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Nater, Alexander
Publications (6 of 6) Show all publications
Bolivar, P., Mugal, C., Sebastiano, M. R., Nater, A., Wang, M., Dutoit, L. & Ellegren, H. (2018). Biased Inference of Selection Due to GC-Biased Gene Conversion and the Rate of Protein Evolution in Flycatchers When Accounting for It. Molecular biology and evolution, 35(10), 2475-2486
Open this publication in new window or tab >>Biased Inference of Selection Due to GC-Biased Gene Conversion and the Rate of Protein Evolution in Flycatchers When Accounting for It
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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
Keywords
d(N)/d(S), distribution of fitness effects, GC-biased gene conversion, gene expression, Hill-Robertson interference
National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-372675 (URN)10.1093/molbev/msy149 (DOI)000452566800011 ()30085180 (PubMedID)
Available from: 2019-01-09 Created: 2019-01-09 Last updated: 2019-04-09Bibliographically approved
Dutoit, L., Burri, R., Nater, A., Mugal, C. F. & Hans, E. (2017). Genomic distribution and estimation of nucleotide diversity in natural populations: perspectives from the collared flycatcher (Ficedula albicollis) genome. Molecular Ecology Resources, 17(4), 586-597
Open this publication in new window or tab >>Genomic distribution and estimation of nucleotide diversity in natural populations: perspectives from the collared flycatcher (Ficedula albicollis) genome
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2017 (English)In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 17, no 4, p. 586-597Article in journal (Refereed) Published
Abstract [en]

Properly estimating genetic diversity in populations of nonmodel species requires a basic understanding of how diversity is distributed across the genome and among individuals. To this end, we analysed whole-genome resequencing data from 20 collared flycatchers (genome size approximate to 1.1 Gb; 10.13 million single nucleotide polymorphisms detected). Genomewide nucleotide diversity was almost identical among individuals (mean = 0.00394, range = 0.00384-0.00401), but diversity levels varied extensively across the genome (95% confidence interval for 200-kb windows = 0.0013-0.0053). Diversity was related to selective constraint such that in comparison with intergenic DNA, diversity at fourfold degenerate sites was reduced to 85%, 3' UTRs to 82%, 5' UTRs to 70% and nondegenerate sites to 12%. There was a strong positive correlation between diversity and chromosome size, probably driven by a higher density of targets for selection on smaller chromosomes increasing the diversity-reducing effect of linked selection. Simulations exploring the ability of sequence data from a small number of genetic markers to capture the observed diversity clearly demonstrated that diversity estimation from finite sampling of such data is bound to be associated with large confidence intervals. Nevertheless, we show that precision in diversity estimation in large out-bred population benefits from increasing the number of loci rather than the number of individuals. Simulations mimicking RAD sequencing showed that this approach gives accurate estimates of genomewide diversity. Based on the patterns of observed diversity and the performed simulations, we provide broad recommendations for how genetic diversity should be estimated in natural populations.

Keywords
genetic markers, nucleotide diversity, population genomics, recombination
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-327358 (URN)10.1111/1755-0998.12602 (DOI)000403258900002 ()
Available from: 2017-08-22 Created: 2017-08-22 Last updated: 2018-02-22Bibliographically approved
Uebbing, S., Künstner, A., Mäkinen, H., Backström, N., Bolivar, P., Burri, R., . . . Ellegren, H. (2016). Divergence in gene expression within and between two closely related flycatcher species. Molecular Ecology, 25(9), 2015-2028
Open this publication in new window or tab >>Divergence in gene expression within and between two closely related flycatcher species
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2016 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 25, no 9, p. 2015-2028Article in journal (Refereed) Published
Abstract [en]

Relatively little is known about the character of gene expression evolution as species diverge. It is for instance unclear if gene expression generally evolves in a clock-like manner (by stabilizing selection or neutral evolution) or if there are frequent episodes of directional selection. To gain insights into the evolutionary divergence of gene expression, we sequenced and compared the transcriptomes of multiple organs from population samples of collared (Ficedula albicollis) and pied flycatchers (F. hypoleuca), two species which diverged less than one million years ago. Ordination analysis separated samples by organ rather than by species. Organs differed in their degrees of expression variance within species and expression divergence between species. Variance was negatively correlated with expression breadth and protein interactivity, suggesting that pleiotropic constraints reduce gene expression variance within species. Variance was correlated with between-species divergence, consistent with a pattern expected from stabilizing selection and neutral evolution. Using an expression PST approach, we identified genes differentially expressed between species and found 16 genes uniquely expressed in one of the species. For one of these, DPP7, uniquely expressed in collared flycatcher, the absence of expression in pied flycatcher could be associated with a ≈ 20 kb deletion including 11 out of 13 exons. This study of a young vertebrate speciation model system expands our knowledge of how gene expression evolves as natural populations become reproductively isolated.

Keywords
collared flycatcher; Ficedula; gene regulation; pied flycatcher; speciation; transcriptomics
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-280030 (URN)10.1111/mec.13596 (DOI)000377023400010 ()26928872 (PubMedID)
Funder
Swedish Research Council, 2010-5650 2013-8271EU, European Research Council, AdG 249976Knut and Alice Wallenberg FoundationWellcome trust, WT095908 WT098051
Available from: 2016-03-07 Created: 2016-03-07 Last updated: 2018-02-22Bibliographically approved
Smeds, L., Warmuth, V., Bolivar, P., Uebbing, S., Burri, R., Suh, A., . . . Ellegren, H. (2015). Evolutionary analysis of the female-specific avian W chromosome. Nature Communications, 6, Article ID 7330.
Open this publication in new window or tab >>Evolutionary analysis of the female-specific avian W chromosome
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2015 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 6, article id 7330Article in journal (Refereed) Published
Abstract [en]

The typically repetitive nature of the sex-limited chromosome means that it is often excluded from or poorly covered in genome assemblies, hindering studies of evolutionary and population genomic processes in non-recombining chromosomes. Here, we present a draft assembly of the non-recombining region of the collared flycatcher W chromosome, containing 46 genes without evidence of female-specific functional differentiation. Survival of genes during W chromosome degeneration has been highly non-random and expression data suggest that this can be attributed to selection for maintaining gene dose and ancestral expression levels of essential genes. Re-sequencing of large population samples revealed dramatically reduced levels of within-species diversity and elevated rates of between-species differentiation (lineage sorting), consistent with low effective population size. Concordance between W chromosome and mitochondrial DNA phylogenetic trees demonstrates evolutionary stable matrilineal inheritance of this nuclear-cytonuclear pair of chromosomes. Our results show both commonalities and differences between W chromosome and Y chromosome evolution.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-259122 (URN)10.1038/ncomms8330 (DOI)000357172100013 ()26040272 (PubMedID)
Funder
Knut and Alice Wallenberg FoundationSwedish Research Council, 2007-8731, 2010-5650, 2013-8271
Available from: 2015-07-28 Created: 2015-07-27 Last updated: 2018-02-22Bibliographically approved
Burri, R., Nater, A., Kawakami, T., Mugal, C. F., Ólason, P. I., Smeds, L., . . . Ellegren, H. (2015). Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Research, 25(11), 1656-1665
Open this publication in new window or tab >>Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers
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2015 (English)In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 25, no 11, p. 1656-1665Article in journal (Refereed) Published
Abstract [en]

Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d(XY) relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-268800 (URN)10.1101/gr.196485.115 (DOI)000364355600007 ()26355005 (PubMedID)
Funder
EU, European Research Council, AdG 249976Knut and Alice Wallenberg FoundationSwedish Research Council, 2010-5650Swedish Research Council, 80576801Swedish Research Council, 70374401Science for Life Laboratory - a national resource center for high-throughput molecular bioscience
Available from: 2015-12-09 Created: 2015-12-09 Last updated: 2018-02-22Bibliographically approved
Nater, A., Burri, R., Kawakami, T., Smeds, L. & Ellegren, H. (2015). Resolving Evolutionary Relationships in Closely Related Species with Whole-Genome Sequencing Data. Systematic Biology, 64(6), 1000-1017
Open this publication in new window or tab >>Resolving Evolutionary Relationships in Closely Related Species with Whole-Genome Sequencing Data
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2015 (English)In: Systematic Biology, ISSN 1063-5157, E-ISSN 1076-836X, Vol. 64, no 6, p. 1000-1017Article in journal (Refereed) Published
Abstract [en]

Using genetic data to resolve the evolutionary relationships of species is of major interest in evolutionary and systematic biology. However, reconstructing the sequence of speciation events, the so-called species tree, in closely related and potentially hybridizing species is very challenging. Processes such as incomplete lineage sorting and interspecific gene flow result in local gene genealogies that differ in their topology from the species tree, and analyses of few loci with a single sequence per species are likely to produce conflicting or even misleading results. To study these phenomena on a full phylogenomic scale, we use whole-genome sequence data from 200 individuals of four black-and-white flycatcher species with so far unresolved phylogenetic relationships to infer gene tree topologies and visualize genome-wide patterns of gene tree incongruence. Using phylogenetic analysis in nonoverlapping 10-kb windows, we show that gene tree topologies are extremely diverse and change on a very small physical scale. Moreover, we find strong evidence for gene flow among flycatcher species, with distinct patterns of reduced introgression on the Z chromosome. To resolve species relationships on the background of widespread gene tree incongruence, we used four complementary coalescent-based methods for species tree reconstruction, including complex modeling approaches that incorporate post-divergence gene flow among species. This allowed us to infer the most likely species tree with high confidence. Based on this finding, we show that regions of reduced effective population size, which have been suggested as particularly useful for species tree inference, can produce positively misleading species tree topologies. Our findings disclose the pitfalls of using loci potentially under selection as phylogenetic markers and highlight the potential of modeling approaches to disentangle species relationships in systems with large effective population sizes and post-divergence gene flow.

Keywords
Approximate Bayesian computation, demographic modeling, gene flow, gene tree, incomplete lineage sorting, introgression, phylogenomics, species tree
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-267189 (URN)10.1093/sysbio/syv045 (DOI)000363168100009 ()26187295 (PubMedID)
Funder
EU, European Research CouncilKnut and Alice Wallenberg FoundationSwedish Research Council, 2007-8731Swedish Research Council, 2010-5650Swedish Research Council, 2013-8271
Available from: 2015-11-20 Created: 2015-11-19 Last updated: 2018-02-22Bibliographically approved
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