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The genomic signatures of adaptive evolution in Populus
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. (Evolutionary biology)ORCID iD: 0000-0002-3793-3264
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Understanding the genetic basis of adaptive evolution, and how natural selection has shaped patterns of polymorphism and divergence within and between species are enduring goals of evolutionary genetics. In this thesis, I used whole genome re-sequencing data to characterize the genomic signatures of natural selection along different evolutionary timescales in three Populus species: Populus tremula, P. tremuloides and P. trichocarpa. First, our study shows multiple lines of evidence suggesting that natural selection, due to both positive and purifying selection, has widely shaped patterns of nucleotide polymorphism at linked neutral sites in all three species. Differences in effective population sizes and rates of recombination largely explain the disparate magnitudes and signatures of linked selection that we observe among species. Second, we characterize the evolution of genomic divergence patterns between two recently diverged aspen species: P. tremula and P. tremuloides. Our findings indicate that the two species diverged ~2.2-3.1 million years ago, coinciding with the severing of the Bering land bridge and the onset of dramatic climatic oscillations during the Pleistocene. We further explore different mechanisms that may explain the heterogeneity of genomic divergence, and find that variation in linked selection and recombination likely plays a key role in generating the heterogeneous genomic landscape of differentiation between the two aspen species. Third, we link whole-genome polymorphic data with local environmental variables and phenotypic variation in an adaptive trait to investigate the genomic basis of local adaptation in P. tremula along a latitudinal gradient across Sweden. We find that a majority of single nucleotide polymorphisms (SNPs) (>90%) identified as being involved in local adaptation are tightly clustered in a single genomic region on chromosome 10. The signatures of selection at this region are more consistent with soft rather than hard selective sweeps, where multiple adaptive haplotypes derived from standing genetic variation sweep through the populations simultaneously, and where different haplotypes rise to high frequency in different latitudinal regions. In summary, this thesis uses phylogenetic comparative approaches to elucidate how various evolutionary forces have shaped genome-wide patterns of sequence evolution in Populus.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2016. , 52 p.
Keyword [en]
Populus, adaptive evolution, natural selection, genomic diversity and divergence, recombination, Next-generation sequencing, local adaptation
National Category
Ecology
Identifiers
URN: urn:nbn:se:umu:diva-120286ISBN: 978-91-7601-463-9 (print)OAI: oai:DiVA.org:umu-120286DiVA: diva2:927986
Public defence
2016-06-08, KB3B1, KBC-huset, Umeå, 13:00 (English)
Opponent
Supervisors
Note

The research in this thesis was supported by the Swedish research council (to Pär K. Ingvarsson) and the JC Kempe Memorial Scholarship Foundation (to Jing Wang). The PhD study of Jing Wang in Sweden was funded by the State Scholarship from China Scholarship council.

Available from: 2016-05-18 Created: 2016-05-13 Last updated: 2016-05-26Bibliographically approved
List of papers
1. Variant calling using NGS data in European aspen (Populus tremula)
Open this publication in new window or tab >>Variant calling using NGS data in European aspen (Populus tremula)
2015 (English)In: Advances in the Understanding of Biological Sciences Using Next Generation Sequencing (NGS) Approaches / [ed] Sablok, G., Kumar, S., Ueno, S., Kuo, J., Varotto, C. (Eds.), Springer, 2015, 1, 43-61 p.Chapter in book (Refereed)
Abstract [en]

Analysis of next-generation sequencing (NGS) data is rapidly becoming an important source of information for genetics and genomics studies. The utility of such data does, however, rely crucially on the accuracy and quality of SNP and genotype calling. Identification of genetic variants (SNPs and short indels) from NGS data is an area of active research and many recent statistical methods have been developed to both improve and quantify the large uncertainty associated with genotype calling. The detection of genetic variants from NGS data is prone to errors, due to multiple factors such as base-calling, alignment errors and read coverage. Here we highlight some of the issues and review and exemplify some of the recent methods that have been developed for genotype calling. We also provide guidelines for their application to whole-genome re-sequencing data using a data set based on a number of European aspen (Populus tremula) individuals each sequenced to a depth of about 20x coverage per individual.

Place, publisher, year, edition, pages
Springer, 2015 Edition: 1
Keyword
Next generation sequencing, variant calling, single nucleotide polymorphism (SNP), pre-processing, alignment, post-processing, filtering
National Category
Biological Sciences
Identifiers
urn:nbn:se:umu:diva-102803 (URN)10.1007/978-3-319-17157-9_4 (DOI)978-3-319-17156-2 (ISBN)
Available from: 2015-05-05 Created: 2015-05-05 Last updated: 2016-05-16Bibliographically approved
2. Natural Selection and Recombination Rate Variation Shape Nucleotide Polymorphism Across the Genomes of Three Related Populus Species
Open this publication in new window or tab >>Natural Selection and Recombination Rate Variation Shape Nucleotide Polymorphism Across the Genomes of Three Related Populus Species
2016 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 202, no 3, 1185-1200 p.Article in journal (Refereed) Published
Abstract [en]

A central aim of evolutionary genomics is to identify the relative roles that various evolutionary forces have played in generating and shaping genetic variation within and among species. Here we use whole-genome resequencing data to characterize and compare genome-wide patterns of nucleotide polymorphism, site frequency spectrum, and population-scaled recombination rates in three species of PopulusPopulus tremulaP. tremuloides, and P. trichocarpa. We find that P. tremuloides has the highest level of genome-wide variation, skewed allele frequencies, and population-scaled recombination rates, whereas P. trichocarpa harbors the lowest. Our findings highlight multiple lines of evidence suggesting that natural selection, due to both purifying and positive selection, has widely shaped patterns of nucleotide polymorphism at linked neutral sites in all three species. Differences in effective population sizes and rates of recombination largely explain the disparate magnitudes and signatures of linked selection that we observe among species. The present work provides the first phylogenetic comparative study on a genome-wide scale in forest trees. This information will also improve our ability to understand how various evolutionary forces have interacted to influence genome evolution among related species.

Place, publisher, year, edition, pages
Genetics Society of America, 2016
Keyword
Populus, whole-genome resequencing, nucleotide polymorphism, recombination, natural selection
National Category
Natural Sciences Evolutionary Biology Genetics
Research subject
Genetics
Identifiers
urn:nbn:se:umu:diva-117941 (URN)10.1534/genetics.115.183152 (DOI)000371596400026 ()
Available from: 2016-03-07 Created: 2016-03-07 Last updated: 2017-11-30Bibliographically approved
3. Variation in linked selection and recombination drive genomic divergence during allopatric speciation of European and American aspens
Open this publication in new window or tab >>Variation in linked selection and recombination drive genomic divergence during allopatric speciation of European and American aspens
2016 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 33, no 7, 1754-1767 p.Article in journal (Refereed) Published
Abstract [en]

Despite the global economic and ecological importance of forest trees, the genomic basis of differential adaptation and speciation in tree species is still poorly understood. Populus tremula and P. tremuloides are two of the most widespread tree species in the Northern Hemisphere. Using whole-genome re-sequencing data of 24 P. tremula and 22 P. tremuloidesindividuals, we find that the two species diverged ~2.2-3.1 million years ago, coinciding with the severing of the Bering land bridge and the onset of dramatic climatic oscillations during the Pleistocene. Both species have experienced substantial population expansions following long-term declines after species divergence. We detect widespread and heterogeneous genomic differentiation between species, and in accordance with the expectation of allopatric speciation, coalescent simulations suggest that neutral evolutionary processes can account for most of the observed patterns of genetic differentiation. However, there is an excess of regions exhibiting extreme differentiation relative to those expected under demographic simulations, which is indicative of the action of natural selection. Overall genetic differentiation is negatively associated with recombination rate in both species, providing strong support for a role of linked selection in generating the heterogeneous genomic landscape of differentiation between species. Finally, we identify a number of candidate regions and genes that may have been subject to positive and/or balancing selection during the speciation process.

Keyword
Populus tremula, P. tremuloides, whole-genome re-sequencing, demographic histories, heterogeneous genomic differentiation, linked selection, recombination
National Category
Evolutionary Biology
Research subject
Genetics; evolutionär genetik
Identifiers
urn:nbn:se:umu:diva-118326 (URN)10.1093/molbev/msw051 (DOI)000378767100009 ()
Available from: 2016-03-16 Created: 2016-03-16 Last updated: 2017-11-30Bibliographically approved
4. The signatures of local adaptation at the genomic level in European aspen (Populus tremula)
Open this publication in new window or tab >>The signatures of local adaptation at the genomic level in European aspen (Populus tremula)
Show others...
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Although local adaptation plays a fundamental role in maintaining adaptive genetic variation as a response to changing environments, its underlying genetic mechanisms remains poorly understood. In this study, we integrate “top-down” and “bottom-up” approaches to search for genomic signatures of local adaptation in Populus tremula along a latitudinal gradient across Sweden. We find that a majority of single nucleotide polymorphisms (SNPs) (~95%) identified as being involved in local adaptation are tightly clustered in a single genomic region on chromosome 10. This region harbors the candidate gene FLOWERING LOCUS T2 (FT2) that has long been known to play important roles in the regulation of growth cessation and dormancy induction in perennial plants. Our results provide empirical evidence suggesting that in the context of high rates of gene flow, the genomic architecture of local adaptation tends to enrich for few large-effect and/or tightly clustered loci rather than many independent loci of small effect. The signatures of selection at the candidate region are mostly consistent with soft selective sweeps, where different adaptive haplotypes originating from standing genetic variation sweep to high frequency in different latitudinal regions. In particular, we identify a recent and strong selective sweep that is regionally restricted to the northernmost populations. This indicates that high-latitude populations likely have undergone a stronger adaptive response to the greater environmental perturbation during the post-glacial colonization of northern Scandinavia.

National Category
Genetics Evolutionary Biology
Identifiers
urn:nbn:se:umu:diva-120279 (URN)
Available from: 2016-05-13 Created: 2016-05-13 Last updated: 2016-05-16

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