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  • 1. Brandvain, Yaniv
    et al.
    Slotte, Tanja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Hazzouri, Khaled M.
    Wright, Stephen I.
    Coop, Graham
    Genomic Identification of Founding Haplotypes Reveals the History of the Selfing Species Capsella rubella2013In: PLOS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 9, no 9, p. e1003754-Article in journal (Refereed)
    Abstract [en]

    The shift from outcrossing to self-fertilization is among the most common evolutionary transitions in flowering plants. Until recently, however, a genome-wide view of this transition has been obscured by both a dearth of appropriate data and the lack of appropriate population genomic methods to interpret such data. Here, we present a novel population genomic analysis detailing the origin of the selfing species, Capsella rubella, which recently split from its outcrossing sister, Capsella grandiflora. Due to the recency of the split, much of the variation within C. rubella is also found within C. grandiflora. We can therefore identify genomic regions where two C. rubella individuals have inherited the same or different segments of ancestral diversity (i.e. founding haplotypes) present in C. rubella's founder(s). Based on this analysis, we show that C. rubella was founded by multiple individuals drawn from a diverse ancestral population closely related to extant C. grandiflora, that drift and selection have rapidly homogenized most of this ancestral variation since C. rubella's founding, and that little novel variation has accumulated within this time. Despite the extensive loss of ancestral variation, the approximately 25% of the genome for which two C. rubella individuals have inherited different founding haplotypes makes up roughly 90% of the genetic variation between them. To extend these findings, we develop a coalescent model that utilizes the inferred frequency of founding haplotypes and variation within founding haplotypes to estimate that C. rubella was founded by a potentially large number of individuals between 50 and 100 kya, and has subsequently experienced a twenty-fold reduction in its effective population size. As population genomic data from an increasing number of outcrossing/selfing pairs are generated, analyses like the one developed here will facilitate a fine-scaled view of the evolutionary and demographic impact of the transition to self-fertilization.

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  • 2. Gos, Gesseca
    et al.
    Slotte, Tanja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Wright, Stephen I.
    Signatures of balancing selection are maintained at disease resistance loci following mating system evolution and a population bottleneck in the genus Capsella2012In: BMC Evolutionary Biology, E-ISSN 1471-2148, Vol. 12, p. 152-Article in journal (Refereed)
    Abstract [en]

    Background: Population bottlenecks can lead to a loss of variation at disease resistance loci, which could have important consequences for the ability of populations to adapt to pathogen pressure. Alternatively, current or past balancing selection could maintain high diversity, creating a strong heterogeneity in the retention of polymorphism across the genome of bottlenecked populations. We sequenced part of the LRR region of 9 NBS-LRR disease resistance genes in the outcrossing Capsella grandiflora and the recently derived, bottlenecked selfing species Capsella rubella, and compared levels and patterns of nucleotide diversity and divergence with genome-wide reference loci. Results: In strong contrast with reference loci, average diversity at resistance loci was comparable between C. rubella and C. grandiflora, primarily due to two loci with highly elevated diversity indicative of past or present balancing selection. Average between-species differentiation was also reduced at the set of R-genes compared with reference loci, which is consistent with the maintenance of ancestral polymorphism. Conclusions: Historical or ongoing balancing selection on plant disease resistance genes is a likely contributor to the retention of ancestral polymorphism in some regions of the bottlenecked Capella rubella genome.

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  • 3. Qiu, Suo
    et al.
    Zeng, Kai
    Slotte, Tanja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Wright, Stephen
    Charlesworth, Deborah
    Reduced Efficacy of Natural Selection on Codon Usage Bias in Selfing Arabidopsis and Capsella Species2011In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 3, p. 868-880Article in journal (Refereed)
    Abstract [en]

    Population genetic theory predicts that the efficacy of natural selection in a self-fertilizing species should be lower than its outcrossing relatives because of the reduction in the effective population size (N(e)) in the former brought about by inbreeding. However, previous analyses comparing Arabidopsis thaliana (selfer) with A. lyrata (outcrosser) have not found conclusive support for this prediction. In this study, we addressed this issue by examining silent site polymorphisms (synonymous and intronic), which are expected to be informative about changes in N(e). Two comparisons were made: A. thaliana versus A. lyrata and Capsella rubella (selfer) versus C. grandiflora (outcrosser). Extensive polymorphism data sets were obtained by compiling published data from the literature and by sequencing 354 exon loci in C. rubella and 89 additional loci in C. grandiflora. To extract information from the data effectively for studying these questions, we extended two recently developed models in order to investigate detailed selective differences between synonymous codons, mutational biases, and biased gene conversion (BGC), taking into account the effects of recent changes in population size. We found evidence that selection on synonymous codons is significantly weaker in the selfers compared with the outcrossers and that this difference cannot be fully accounted for by mutational biases or BGC.

  • 4.
    Slotte, Tanja
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Bataillon, Thomas
    Hansen, Troels T.
    St. Onge, Kate
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Wright, Stephen I.
    Schierup, Mikkel H.
    Genomic Determinants of Protein Evolution and Polymorphism in Arabidopsis2011In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 3, p. 1210-1219Article in journal (Refereed)
    Abstract [en]

    Recent results from Drosophila suggest that positive selection has a substantial impact on genomic patterns of polymorphism and divergence. However, species with smaller population sizes and/or stronger population structure may not be expected to exhibit Drosophila-like patterns of sequence variation. We test this prediction and identify determinants of levels of polymorphism and rates of protein evolution using genomic data from Arabidopsis thaliana and the recently sequenced Arabidopsis lyrata genome. We find that, in contrast to Drosophila, there is no negative relationship between nonsynonymous divergence and silent polymorphism at any spatial scale examined. Instead, synonymous divergence is a major predictor of silent polymorphism, which suggests variation in mutation rate as the main determinant of silent variation. Variation in rates of protein divergence is mainly correlated with gene expression level and breadth, consistent with results for a broad range of taxa, and map-based estimates of recombination rate are only weakly correlated with nonsynonymous divergence. Variation in mutation rates and the strength of purifying selection seem to be major drivers of patterns of polymorphism and divergence in Arabidopsis. Nevertheless, a model allowing for varying negative and positive selection by functional gene category explains the data better than a homogeneous model, implying the action of positive selection on a subset of genes. Genes involved in disease resistance and abiotic stress display high proportions of adaptive substitution. Our results are important for a general understanding of the determinants of rates of protein evolution and the impact of selection on patterns of polymorphism and divergence.

  • 5.
    Slotte, Tanja
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Hazzouri, Khaled M.
    Agren, J. Arvid
    Koenig, Daniel
    Maumus, Florian
    Guo, Ya-Long
    Steige, Kim
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Platts, Adrian E.
    Escobar, Juan S.
    Newman, L. Killian
    Wang, Wei
    Mandakova, Terezie
    Vello, Emilio
    Smith, Lisa M.
    Henz, Stefan R.
    Steffen, Joshua
    Takuno, Shohei
    Brandvain, Yaniv
    Coop, Graham
    Andolfatto, Peter
    Hu, Tina T.
    Blanchette, Mathieu
    Clark, Richard M.
    Quesneville, Hadi
    Nordborg, Magnus
    Gaut, Brandon S.
    Lysak, Martin A.
    Jenkins, Jerry
    Grimwood, Jane
    Chapman, Jarrod
    Prochnik, Simon
    Shu, Shengqiang
    Rokhsar, Daniel
    Schmutz, Jeremy
    Weigel, Detlef
    Wright, Stephen I.
    The Capsella rubella genome and the genomic consequences of rapid mating system evolution2013In: Nature Genetics, ISSN 1061-4036, E-ISSN 1546-1718, Vol. 45, no 7, p. 831-U165Article in journal (Refereed)
    Abstract [en]

    The shift from outcrossing to selfing is common in flowering plants(1,2), but the genomic consequences and the speed at which they emerge remain poorly understood. An excellent model for understanding the evolution of self fertilization is provided by Capsella rubella, which became self compatible <200,000 years ago. We report a C. rubella reference genome sequence and compare RNA expression and polymorphism patterns between C. rubella and its outcrossing progenitor Capsella grandiflora. We found a clear shift in the expression of genes associated with flowering phenotypes, similar to that seen in Arabidopsis, in which self fertilization evolved about 1 million years ago. Comparisons of the two Capsella species showed evidence of rapid genome-wide relaxation of purifying selection in C. rubella without a concomitant change in transposable element abundance. Overall we document that the transition to selfing may be typified by parallel shifts in gene expression, along with a measurable reduction of purifying selection.

  • 6.
    Slotte, Tanja
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Hazzouri, Khaled M.
    Stern, David
    Andolfatto, Peter
    Wright, Stephen I.
    Genetic architecture and adaptive significance of the selfing syndrome in Capsella2012In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 66, no 5, p. 1360-1374Article in journal (Refereed)
    Abstract [en]

    The transition from outcrossing to predominant self-fertilization is one of the most common evolutionary transitions in flowering plants. This shift is often accompanied by a suite of changes in floral and reproductive characters termed the selfing syndrome. Here, we characterize the genetic architecture and evolutionary forces underlying evolution of the selfing syndrome in Capsella rubella following its recent divergence from the outcrossing ancestor C. grandiflora. We conduct genotyping by multiplexed shotgun sequencing and map floral and reproductive traits in a large (N= 550) F2 population. Our results suggest that in contrast to previous studies of the selfing syndrome, changes at a few loci, some with major effects, have shaped the evolution of the selfing syndrome in Capsella. The directionality of QTL effects, as well as population genetic patterns of polymorphism and divergence at 318 loci, is consistent with a history of directional selection on the selfing syndrome. Our study is an important step toward characterizing the genetic basis and evolutionary forces underlying the evolution of the selfing syndrome in a genetically accessible model system.

  • 7.
    Slotte, Tanja
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Functional Genomics.
    Holm, Karl
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Functional Genomics.
    McIntyre, Lauren
    Department of Molecular Genetics and Microbiology, University of Florida.
    Lagercrantz, Ulf
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Functional Genomics.
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Evolution, Genomics and Systematics, Evolutionary Functional Genomics.
    Differential expression of genes important for adaptation in Capsella bursa-pastoris (Brassicaceae)2007In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 145, no 1, p. 160-173Article, review/survey (Refereed)
    Abstract [en]

    Understanding the genetic basis of natural variation is of primary interest for evolutionary studies of adaptation. In Capsella bursa-pastoris, a close relative of Arabidopsis (Arabidopsis thaliana), variation in flowering time is correlated with latitude, suggestive of an adaptation to photoperiod. To identify pathways regulating natural flowering time variation in C. bursa-pastoris, we have studied gene expression differences between two pairs of early- and late-flowering C. bursa-pastoris accessions and compared their response to vernalization. Using Arabidopsis microarrays, we found a large number of significant differences in gene expression between flowering ecotypes. The key flowering time gene FLOWERING LOCUS C (FLC) was not differentially expressed prior to vernalization. This result is in contrast to those in Arabidopsis, where most natural flowering time variation acts through FLC. However, the gibberellin and photoperiodic flowering pathways were significantly enriched for gene expression differences between early- and late-flowering C. bursa-pastoris. Gibberellin biosynthesis genes were downregulated in late-flowering accessions, whereas circadian core genes in the photoperiodic pathway were differentially expressed between early- and late-flowering accessions. Detailed time-series experiments clearly demonstrated that the diurnal rhythm of CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) and TIMING OF CAB EXPRESSIONI (TOC1) expression differed between flowering ecotypes, both under constant light and long-day conditions. Differential expression of flowering time genes was biologically validated in an independent pair of flowering ecotypes, suggesting a shared genetic basis or parallel evolution of similar regulatory differences. We conclude that genes involved in regulation of the circadian clock, such as CCA1 and TOC1, are strong candidates for the evolution of adaptive flowering time variation in C. bursa-pastoris.

  • 8.
    St Onge, Kate
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Foxe, John Paul
    Department of Biology, York University.
    Li, Junrui
    Laboratory of Evolutionary Genomics, CAS-MPG Partner Institute for Computational Biology, Chinese Academy of Sciences.
    Li, Haipeng
    Laboratory of Evolutionary Genomics, CAS-MPG Partner Institute for Computational Biology, Chinese Academy of Sciences.
    Holm, Karl
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Corcoran, Pádraic
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Tanja, Slotte
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Lascoux, Martin
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Plant Ecology and Evolution.
    Stephen, Wright
    Department of Ecology and Evolutionary Biology, University of Toronto.
    Coalescent-based analysis distinguishes between allo- and autopolyploid origin in shepherd’s purse (Capsella bursa-pastoris)2012In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 29, no 7, p. 1721-1733Article in journal (Refereed)
    Abstract [en]

    Polyploidization plays an important role in plant speciation. The most recent estimates 36 report that up to 15% of angiosperm speciation events and 31% in ferns are accompanied 37 by changes in ploidy level. Polyploids can arise either through autopolyploidy, when the 38 sets of chromosomes originate from a single species, or through allopolyploidy, when 39 they originate from different species. In this study we used two different coalescent-based 40 methods to determine the date and mode of the polyploidization event that led to the 41 tetraploid cosmopolitan weed, Capsella bursa-pastoris. We sampled 78 C. bursa-pastoris 42 accessions, and 53 and 43 accessions from the only two other members of this genus, C. 43 grandiflora and C. rubella, respectively, and sequenced these accessions at 14 unlinked 44 nuclear loci with locus-specific primers in order to be able to distinguish the two 45 homeologues in the tetraploid. A large fraction of fixed differences between 46 homeologous genes in C. bursa-pastoris are segregating as polymorphisms in C. 47 grandiflora, consistent with an autopolyploid origin followed by disomic inheritance. To 48 test this, we first estimated the demographic parameters of an isolation-with-migration 49 model in a pairwise fashion between C. grandiflora and both genomes of C. bursa- 50 pastoris and used these parameters in coalescent simulations to test the mode of origin of 51 C. bursa-pastoris. Secondly we used Approximate Bayesian Computation to compare an 52 allopolyploid and an autopolyploid model. Both analyses led to the conclusion that C. 53 bursa-pastoris originated less than one million years ago by doubling of the C. 54 grandiflora genome.

  • 9.
    Steige, Kim A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Laenen, Benjamin
    Reimegård, Johan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular Evolution. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Scofield, Douglas G.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Slotte, Tanja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Genomic analysis reveals major determinants of cis-regulatory variation in Capsella grandiflora2017In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, Vol. 114, no 5, p. 1087-1092Article in journal (Refereed)
  • 10. Wright, Stephen I.
    et al.
    Kalisz, Susan
    Slotte, Tanja
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Evolutionary consequences of self-fertilization in plants2013In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 280, no 1760, p. 20130133-Article, review/survey (Refereed)
    Abstract [en]

    The transition from outcrossing to self-fertilization is one of the most common evolutionary changes in plants, yet only about 10-15% of flowering plants are predominantly selfing. To explain this phenomenon, Stebbins proposed that selfing may be an 'evolutionary dead end'. According to this hypothesis, transitions from outcrossing to selfing are irreversible, and selfing lineages suffer from an increased risk of extinction owing to a reduced potential for adaptation. Thus, although selfing can be advantageous in the short term, selfing lineages may be mostly short-lived owing to higher extinction rates. Here, we review recent results relevant to the 'dead-end hypothesis' of selfing and the maintenance of outcrossing over longer evolutionary time periods. In particular, we highlight recent results regarding diversification rates in self-incompatible and self-compatible taxa, and review evidence regarding the accumulation of deleterious mutations in selfing lineages. We conclude that while some aspects of the hypothesis of selfing as a dead end are supported by theory and empirical results, the evolutionary and ecological mechanisms remain unclear. We highlight the need for more studies on the effects of quantitative changes in outcrossing rates and on the potential for adaptation, particularly in selfing plants. In addition, there is growing evidence that transitions to selfing may themselves be drivers of speciation, and future studies of diversification and speciation should investigate this further.

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