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Determinants of genomic diversity in the collared flycatcher (Ficedula albicollis)
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Description
Abstract [en]

Individuals vary from each other in their genetic content. Genetic diversity is at the core of the evolutionary theory. Rooted in a solid theoretical framework developed as early as the 1930s, current empirical observations of genomic diversity became possible due to technological advances. These measurements, originally based on a few gene sequences from several individuals, are becoming possible at the genome scale for entire populations. We can now explore how evolutionary forces shape diversity levels along different parts of the genome. In this thesis, I focus on the variation in levels of diversity within genomes using avian systems and in particular that of the collared flycatcher (Ficedula albicollis). First, I describe the variation in genetic diversity along the genome of the collared flycatcher and compare it to the amount of variation in diversity across individuals within the population. I provide guidelines on how a small number of makers can capture the extent of variability in a population. Second, I investigate the stability of the local levels of diversity in the genome across evolutionary time scales by comparing collared flycatcher to the hooded crow (Corvus (corone) corone). Third, I study how selection can maintain variation through pervasive evolutionary conflict between sexes. Lastly, I explore how shifts in genome-wide variant frequencies across few generations can be utilised to estimate the effective size of population.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. , 43 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1582
Keyword [en]
collared flycatcher, Ficedula albicollis, enetic diversity, sexual conflict, effective population size, nucleotide diversity, linked selection
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-331919ISBN: 978-91-513-0120-4 (print)OAI: oai:DiVA.org:uu-331919DiVA: diva2:1150692
Public defence
2017-12-08, Ekmansalen, Norbyvägen 14 A, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2017-11-14 Created: 2017-10-19 Last updated: 2017-11-14
List of papers
1. Genomic distribution and estimation of nucleotide diversity in natural populations: perspectives from the collared flycatcher (Ficedula albicollis) genome
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, 586-597 p.Article 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.

Keyword
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: 2017-10-19Bibliographically approved
2. Covariation in levels of nucleotide diversity in homologous regions of the avian genome long after completion of lineage sorting
Open this publication in new window or tab >>Covariation in levels of nucleotide diversity in homologous regions of the avian genome long after completion of lineage sorting
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2017 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 284, no 1849, 20162756Article in journal (Refereed) Published
Abstract [en]

Closely related species may show similar levels of genetic diversity in homologous regions of the genome owing to shared ancestral variation still segregating in the extant species. However, after completion of lineage sorting, such covariation is not necessarily expected. On the other hand, if the processes that govern genetic diversity are conserved, diversity may potentially covary even among distantly related species. We mapped regions of conserved synteny between the genomes of two divergent bird speciescollared flycatcher and hooded crow-and identified more than 600 Mb of homologous regions (66% of the genome). From analyses of whole-genome resequencing data in large population samples of both species we found nucleotide diversity in 200 kb windows to be well correlated (Spearman's rho = 0.407). The correlation remained highly similar after excluding coding sequences. To explain this covariation, we suggest that a stable avian karyotype and a conserved landscape of recombination rate variation render the diversity-reducing effects of linked selection similar in divergent bird lineages. Principal component regression analysis of several potential explanatory variables driving heterogeneity in flycatcher diversity levels revealed the strongest effects from recombination rate variation and density of coding sequence targets for selection, consistent with linked selection. It is also possible that a stable karyotype is associated with a conserved genomic mutation environment contributing to covariation in diversity levels between lineages. Our observations imply that genetic diversity is to some extent predictable.

Place, publisher, year, edition, pages
ROYAL SOC, 2017
Keyword
nucleotide diversity, linked selection, recombination rate, birds
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-320453 (URN)10.1098/rspb.2016.2756 (DOI)000395893200017 ()
Available from: 2017-04-26 Created: 2017-04-26 Last updated: 2017-10-19Bibliographically approved
3. Sex-biased gene expression, sexual antagonism and levels of genetic diversity in the collared flycatcher (Ficedula albicollis) genome
Open this publication in new window or tab >>Sex-biased gene expression, sexual antagonism and levels of genetic diversity in the collared flycatcher (Ficedula albicollis) genome
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Theoretical work suggests that sexual conflict should promote the maintenance of genetic diversity by the opposing directions of selection on sexually antagonistic mutations in males and females. This prediction, so far not been empirically tested on a genome-wide scale, could potentially contribute towards genomic heterogeneity in levels of genetic diversity. We used large-scale population genomic and transcriptomic data from the collared flycatcher (Ficedula albicollis) to analyse how sex-biased gene expression – one outcome of sexual conflict – relates to genetic variability. Here, we demonstrate that the extent of sex-biased gene expression of both male-biased and female-biased genes is significantly correlated with levels of nucleotide diversity in gene sequences and that this correlation extends to the overall levels of genomic diversity. We find evidence for balancing selection in sex-biased genes, suggesting that sex-biased gene expression could be seen as a component counteracting the diversity-reducing effects of linked positive and purifying selection. The observation of significant genetic differentiation between males and females for male-biased genes indicates ongoing sexual conflict and sex-specific viability selection, potentially driven by sexual selection. Our results thus provide a new perspective on the long-standing question in evolutionary biology of how genomes can remain so genetically variable in face of strong natural and sexual selection.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-331832 (URN)
Available from: 2017-10-18 Created: 2017-10-18 Last updated: 2017-10-19
4. Estimation of contemporary effect population size in an island population of the collared flycatcher (Ficedula albicollis) using large-scale genome data
Open this publication in new window or tab >>Estimation of contemporary effect population size in an island population of the collared flycatcher (Ficedula albicollis) using large-scale genome data
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Due to its central importance to many aspects of evolutionary biology and population genetics, the long-term effective population size (Ne) has been estimated for numerous species and populations. However, estimating contemporary Ne is difficult and in practice this parameter is often not known. In principle, contemporary Ne can be estimated using either analyses of temporal changes in allele frequencies or the extent of linkage disequilibrium (LD) between unlinked markers. We applied these approaches for contemporary Ne estimation of a relatively recently founded island population of collared flycatchers (Ficedula albicollis). We sequenced the genomes of 85 birds sampled in 1993 and 2015, and used a method of Jorde & Ryman (2007) to estimate Ne to ≈5,000 based on the amount of genetic drift observed between the two cohorts. This corresponds to an effective size/census size (Ne/Nc) ratio of ≈0.5. An approach based on LD applied to each cohort could not separate from Ne infinity. When individuals from the two cohorts were pooled, Ne was estimated to 10,000-25,000, but these estimates may be sensitive to biases. We conclude that whole-genome sequence data offer new possibilities for estimation of contemporary Ne, but also note that such estimation remains difficult. 

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-331916 (URN)
Note

Dutoit L and Nadachowska-Brzyska K contributed equally.

Available from: 2017-10-19 Created: 2017-10-19 Last updated: 2017-10-19

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