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Divergence in gene expression within and between two closely related flycatcher species
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.ORCID iD: 0000-0003-2439-6946
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.
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Compared to DNA sequence evolution, relatively little is known about the character of gene expression evolution as species diverge. For example, it is unclear if gene expression generally evolves in a clock-like manner (by stabilizing selection or from neutral evolution) or if there are frequent episodes of directional selection. To gain insights into the evolutionary divergence of gene expression patterns, we sequenced and compared the transcriptomes of multiple tissues from population samples of collared (Ficedula albicollis) and pied flycatchers (F. hypoleuca), a species pair which diverged less than one million years ago. Tissues resolved into separate clusters in non-metric multidimensional scaling ordination analysis and samples from the two species generally clustered by tissue rather than by species. Tissues differed in the degrees of expression variance within species and divergence between species. Variance was positively correlated with expression breadth and negatively correlated with 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 QST approach, we identified genes differentially expressed between species. We also identified 10 genes uniquely expressed in one of the species. For one such gene (DPP7, uniquely expressed in collared flycatcher), the absence of expression in pied flycatchers could be associated with a fixed ≈ 20 kb deletion including 11 out of 13 exons in this species. This study conducted in a young vertebrate speciation model system expands our knowledge of how gene expression evolves in natural populations.

Keyword [en]
Gene regulation, speciation, transcriptomics, collared flycatcher, pied flycatcher, Ficedula
National Category
Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
URN: urn:nbn:se:uu:diva-258798OAI: oai:DiVA.org:uu-258798DiVA: diva2:844293
Available from: 2015-08-04 Created: 2015-07-20 Last updated: 2015-10-01
In thesis
1. On the Evolution of the Avian Transcriptome
Open this publication in new window or tab >>On the Evolution of the Avian Transcriptome
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Change in gene expression is a powerful tool for evolution, because seemingly small expression changes can contribute important steps towards adaptation without necessarily affecting the whole organism. There is still much to learn about how gene expression evolves on genome- and population-wide levels, especially in non-model organisms. This thesis addresses some important questions in gene expression evolution via the quantitative measurement of RNA and protein levels in birds.

First, I confirmed the state of incomplete dosage compensation in birds by sequencing the transcriptome of collared flycatchers (Ficedula albicollis). I showed that pleiotropy governs the evolution of expression male-bias from the Z chromosome. Sex-linked genes in females were more highly expressed than half the male expression level, indicative of a partial up-regulation. A comparison with data from ostrich (Struthio camelus), a bird with non-degenerated sex chromosomes, showed that sex-linked expression male-bias evolved following sex chromosome degradation.

Second, using a combination of RNA sequencing and proteome mass spectrometry in chicken (Gallus gallus), I asked whether complete dosage compensation was achieved through regulation at translation. I showed that this was not the case and that incomplete dosage compensation extends to the protein level in birds. In addition, sex-linked genes showed more often an increased amount of regulation at translational level than autosomal genes.

Third, I investigated gene expression divergence between collared and pied flycatchers (Ficedula hypoleuca) using RNA sequencing in multiple tissues and individuals. Tissues differed in the degree of expression variance and in the number of divergent genes, which I identified using expression QST. Variance within species was negatively correlated with expression breadth and protein interactivity, indicating that evolutionary constraints act predominantly within interbreeding populations. Among genes unique to one of the species, I identified one gene, DPP7, falling into a large genomic deletion fixed in pied flycatchers.

Fourth, I investigated allele-specific expression (ASE) in the two flycatcher populations. ASE was identified from genetic variants within transcripts using RNA sequencing reads. We developed a Bayesian negative binomial approach that gained statistical power by estimating expression variance from combined SNPs within a transcript and overdispersion from the whole dataset.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. 42 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1270
Keyword
evolution, gene expression, regulation, RNA-seq, transcriptomics, proteomics, sex chromosome, dosage compensation, divergence, ASE, birds, Ficedula, flycatcher, chicken
National Category
Biological Sciences Evolutionary Biology Genetics
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-259487 (URN)978-91-554-9292-2 (ISBN)
Public defence
2015-09-24, Ekmansalen, Norbyvägen 14, Uppsala, 13:15 (English)
Supervisors
Available from: 2015-09-02 Created: 2015-08-05 Last updated: 2015-10-01

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Uebbing, Severin

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