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Variation in linked selection and recombination drive genomic divergence during allopatric speciation of European and American aspens
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.ORCID iD: 0000-0002-3793-3264
Umeå University, Faculty of Science and Technology, Department of Plant Physiology.ORCID iD: 0000-0001-6031-005X
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences. Department of Ecology and Genetics: Evolutionary Biology, Uppsala University, Uppsala, Sweden; Uppsala Multidisciplinary Center for Advanced Computational Science, Uppsala University, Uppsala, Sweden.
Umeå University, Faculty of Science and Technology, Department of Ecology and Environmental Sciences.ORCID iD: 0000-0001-9225-7521
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.

Place, publisher, year, edition, pages
2016. Vol. 33, no 7, 1754-1767 p.
Keyword [en]
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: urn:nbn:se:umu:diva-118326DOI: 10.1093/molbev/msw051ISI: 000378767100009OAI: oai:DiVA.org:umu-118326DiVA: diva2:912284
Available from: 2016-03-16 Created: 2016-03-16 Last updated: 2017-11-30Bibliographically approved
In thesis
1. The genomic signatures of adaptive evolution in Populus
Open this publication in new window or tab >>The genomic signatures of adaptive evolution in Populus
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
Populus, adaptive evolution, natural selection, genomic diversity and divergence, recombination, Next-generation sequencing, local adaptation
National Category
Ecology
Identifiers
urn:nbn:se:umu:diva-120286 (URN)978-91-7601-463-9 (ISBN)
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

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Wang, JingStreet, NathanielScofield, DouglasIngvarsson, Pär
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