Genome evolution and adaptation of a successful allopolyploid, Capsella bursa-pastoris

Kryvokhyzha, D. 2018. Genome evolution and adaptation of a successful allopolyploid, Capsella bursa-pastoris. Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology 1632. 51 pp. Uppsala: Acta Universitatis Upsaliensis. ISBN 978-91-513-0236-2. 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.