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Genomic signature of successful colonization of Eurasia by the allopolyploid shepherd's purse (Capsella bursa-pastoris)
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
Univ Toronto, Dept Ecol & Evolutionary Biol, 25 Willcocks St, Toronto, ON M6R 1M3, Canada..
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
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2016 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 25, no 2, p. 616-629Article in journal (Refereed) Published
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Text
Abstract [en]

Polyploidization is a dominant feature of flowering plant evolution. However, detailed genomic analyses of the interpopulation diversification of polyploids following genome duplication are still in their infancy, mainly because of methodological limits, both in terms of sequencing and computational analyses. The shepherd's purse (Capsella bursa-pastoris) is one of the most common weed species in the world. It is highly self-fertilizing, and recent genomic data indicate that it is an allopolyploid, resulting from hybridization between the ancestors of the diploid species Capsella grandiflora and Capsella orientalis. Here, we investigated the genomic diversity of C.bursa-pastoris, its population structure and demographic history, following allopolyploidization in Eurasia. To that end, we genotyped 261 C.bursa-pastoris accessions spread across Europe, the Middle East and Asia, using genotyping-by-sequencing, leading to a total of 4274 SNPs after quality control. Bayesian clustering analyses revealed three distinct genetic clusters in Eurasia: one cluster grouping samples from Western Europe and Southeastern Siberia, the second one centred on Eastern Asia and the third one in the Middle East. Approximate Bayesian computation (ABC) supported the hypothesis that C.bursa-pastoris underwent a typical colonization history involving low gene flow among colonizing populations, likely starting from the Middle East towards Europe and followed by successive human-mediated expansions into Eastern Asia. Altogether, these findings bring new insights into the recent multistage colonization history of the allotetraploid C.bursa-pastoris and highlight ABC and genotyping-by-sequencing data as promising but still challenging tools to infer demographic histories of selfing allopolyploids.

Place, publisher, year, edition, pages
2016. Vol. 25, no 2, p. 616-629
Keyword [en]
Brassicaceae, time estimation, invasive species, dispersal, bottleneck, disomic inheritance, unphased SNP
National Category
Botany Genetics
Identifiers
URN: urn:nbn:se:uu:diva-279642DOI: 10.1111/mec.13491ISI: 000369530000013PubMedID: 26607306OAI: oai:DiVA.org:uu-279642DiVA, id: diva2:909988
Funder
Swedish Research Council
Available from: 2016-03-08 Created: 2016-03-02 Last updated: 2018-02-13Bibliographically approved
In thesis
1. Genome evolution and adaptation of a successful allopolyploid, Capsella bursa-pastoris
Open this publication in new window or tab >>Genome evolution and adaptation of a successful allopolyploid, Capsella bursa-pastoris
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The term allopolyploid refers to an organism that originated through hybridization and increased its ploidy level by retaining the unreduced genomes of its parents. Both hybridization and polyploidy usually have negative consequences for the organism. However, there are species that not only survive these modifications but even thrive and can outcompete their diploid relatives. There are many intuitive explanations for the success of polyploids, but the number of empirical studies is limited.

The shepherd's purse (Capsella bursa-pastoris) is an emerging model for studying a successful allopolyploid species. C. bursa-pastoris occurs worldwide, whereas its parental species, Capsella grandiflora and Capsella orientalis, have more limited distribution range. C. grandiflora is confined to Northern Greece and Albania, and C. orientalis is found only in the steppes of Central Asia. We described the genetic variation within C. bursa-pastoris and showed that it is not homogeneous across Eurasia but rather subdivided into three genetically distinct populations: one comprises accessions from Europe and Eastern Siberia, the second one is located in Eastern Asia and the third one groups accessions around the Middle East. Reconstruction of the colonization history suggested that this species originated in the Middle East and subsequently spread to Europe and Eastern Asia. This colonization was probably human-mediated. Interestingly, these three populations survive in different environmental conditions, and yet most gene expression differences between them could be explained by neutral processes. We also found that despite a common history within one species, the two subgenomes retained differences already present between the parental species. In particular, the genetic load was still higher on the subgenome inherited from C. orientalis than on the one inherited from C. grandiflora. The two subgenomes were also differentially influenced by introgression and selection in the three genetic clusters. Gene expression variation was highly correlated between the two subgenomes but the total level of expression showed variation in parental dominance across flower, leaf, and root tissues.

This thesis for the first time shows that the evolutionary pathways of allopolyploids may differ not only on the species level but also between populations within one species. It also supports the theory that alloploidy provides an increased amount of genetic material that enables evolutionary flexibility.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2018. p. 51
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1632
Keyword
allopolyploidy, population structure, selection, genetic drift, gene expression, parental legacy, genetic load
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Functional Genomics
Identifiers
urn:nbn:se:uu:diva-341709 (URN)978-91-513-0236-2 (ISBN)
Public defence
2018-03-27, Lindhalsalen, Norbyväagen 18, Uppsala, 10:00 (English)
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Supervisors
Available from: 2018-03-05 Created: 2018-02-13 Last updated: 2018-04-03

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Kryvokhyzha, DmytroGlemin, SylvainLascoux, Martin

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