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Clergeot, P.-H., Rode, N. O., Glemin, S., Durling, M. B., Ihrmark, K. & Olson, A. (2019). Estimating the Fitness Effect of Deleterious Mutations During the Two Phases of the Life Cycle: A New Method Applied to the Root-Rot Fungus Heterobasidion parviporum. Genetics, 211(3), 963-976
Open this publication in new window or tab >>Estimating the Fitness Effect of Deleterious Mutations During the Two Phases of the Life Cycle: A New Method Applied to the Root-Rot Fungus Heterobasidion parviporum
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2019 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 211, no 3, p. 963-976Article in journal (Refereed) Published
Abstract [en]

Many eukaryote species, including taxa such as fungi or algae, have a lifecycle with substantial haploid and diploid phases. A recent theoretical model predicts that such haploid-diploid lifecycles are stable over long evolutionary time scales when segregating deleterious mutations have stronger effects in homozygous diploids than in haploids and when they are partially recessive in heterozygous diploids. The model predicts that effective dominance-a measure that accounts for these two effects-should be close to 0.5 in these species. It also predicts that diploids should have higher fitness than haploids on average. However, an appropriate statistical framework to conjointly investigate these predictions is currently lacking. In this study, we derive a new quantitative genetic model to test these predictions using fitness data of two haploid parents and their diploid offspring, and genome-wide genetic distance between haploid parents. We apply this model to the root-rot basidiomycete fungus Heterobasidion parviporum-a species where the heterokaryotic (equivalent to the diploid) phase is longer than the homokaryotic (haploid) phase. We measured two fitness-related traits (mycelium growth rate and the ability to degrade wood) in both homokaryons and heterokaryons, and we used whole-genome sequencing to estimate nuclear genetic distance between parents. Possibly due to a lack of power, we did not find that deleterious mutations were recessive or more deleterious when expressed during the heterokaryotic phase. Using this model to compare effective dominance among haploid-diploid species where the relative importance of the two phases varies should help better understand the evolution of haploid-diploid life cycles.

Keywords
homokaryon, heterokaryon, mycelium growth rate, wood degradation, genetic distance, dominance, epistasis, biphasic life cycle, mitochondria
National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-379924 (URN)10.1534/genetics.118.301855 (DOI)000460597200011 ()30598467 (PubMedID)
Funder
Swedish Foundation for Strategic Research , RBb08-0011
Available from: 2019-03-27 Created: 2019-03-27 Last updated: 2019-03-27Bibliographically approved
Tahir, D., Glemin, S., Lascoux, M. & Kaj, I. (2019). Modeling a trait-dependent diversification process coupled with molecular evolution on a random species tree. Journal of Theoretical Biology, 461, 189-203
Open this publication in new window or tab >>Modeling a trait-dependent diversification process coupled with molecular evolution on a random species tree
2019 (English)In: Journal of Theoretical Biology, ISSN 0022-5193, E-ISSN 1095-8541, Vol. 461, p. 189-203Article in journal (Refereed) Published
Abstract [en]

Understanding the evolution of binary traits, which affects the birth and survival of species and also the rate of molecular evolution, remains challenging. In this work, we present a probabilistic modeling framework for binary trait, random species trees, in which the number of species and their traits are represented by an asymmetric, two-type, continuous time Markov branching process. The model involves a number of different parameters describing both character and molecular evolution on the so-called 'reduced' tree, consisting of only extant species at the time of observation. We expand our model by considering the impact of binary traits on dN/dS, the normalized ratio of nonsynonymous to synonymous substitutions. We also develop mechanisms which enable us to understand the substitution rates on a phylogenetic tree with regards to the observed traits. The properties obtained from the model are illustrated with a phylogeny of outcrossing and selfing plant species, which allows us to investigate not only the branching tree rates, but also the molecular rates and the intensity of selection.

Keywords
Branching processes, Irreversible transitions, Binary traits, Phylogenetic trees, Mutation rates
National Category
Evolutionary Biology Probability Theory and Statistics
Identifiers
urn:nbn:se:uu:diva-372749 (URN)10.1016/j.jtbi.2018.10.032 (DOI)000452245900018 ()30340056 (PubMedID)
Available from: 2019-01-15 Created: 2019-01-15 Last updated: 2019-04-25
Kryvokhyzha, D., Salcedo, A., Eriksson, M. C., Duan, T., Tawari, N., Chen, J., . . . Lascoux, M. (2019). Parental legacy, demography, and admixture influenced the evolution of the two subgenomes of the tetraploid Capsella bursa-pastoris (Brassicaceae). PLoS Genetics, 15(2), Article ID e1007949.
Open this publication in new window or tab >>Parental legacy, demography, and admixture influenced the evolution of the two subgenomes of the tetraploid Capsella bursa-pastoris (Brassicaceae)
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2019 (English)In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 15, no 2, article id e1007949Article in journal (Refereed) Published
Abstract [en]

Allopolyploidy is generally perceived as a major source of evolutionary novelties and as an instantaneous way to create isolation barriers. However, we do not have a clear understanding of how two subgenomes evolve and interact once they have fused in an allopolyploid species nor how isolated they are from their relatives. Here, we address these questions by analyzing genomic and transcriptomic data of allotetraploid Capsella bursa-pastoris in three differentiated populations, Asia, Europe, and the Middle East. We phased the two subgenomes, one descended from the outcrossing and highly diverse Capsella grandiflora (Cbp(Cg)) and the other one from the selfing and genetically depauperate Capsella orientalis (Cbp(Co)). For each subgenome, we assessed its relationship with the diploid relatives, temporal changes of effective population size (N-e), signatures of positive and negative selection, and gene expression patterns. In all three regions, N-e of the two subgenomes decreased gradually over time and the Cbp(Co) subgenome accumulated more deleterious changes than Cbp(Cg). There were signs of widespread admixture between C. bursa-pastoris and its diploid relatives. The two subgenomes were impacted differentially depending on geographic region suggesting either strong interploidy gene flow or multiple origins of C. bursa-pastoris. Selective sweeps were more common on the Cbp(Cg) subgenome in Europe and the Middle East, and on the Cbp(Co) subgenome in Asia. In contrast, differences in expression were limited with the Cbp(Cg) subgenome slightly more expressed than Cbp(Co) in Europe and the Middle-East. In summary, after more than 100,000 generations of co-existence, the two subgenomes of C. bursa-pastoris still retained a strong signature of parental legacy but their evolutionary trajectory strongly varied across geographic regions. Author summary Allopolyploid species have two or more sets of chromosomes that originate from hybridization of different species. It remains largely unknown how the two genomes evolve in the same organism and how strongly their evolutionary trajectory depends on the initial differences between the two parental species and the specific demographic history of the newly formed allopolyploid species. To address these questions, we analyzed the genomic and gene expression variation of the shepherd's purse, a recent allopolyploid species, in three regions of its natural range. After approximate to 100,000 generations of co-existence within the same species, the two subgenomes had still retained part of the initial difference between the two parental species in the number of deleterious mutations reflecting a history of mating system differences. This difference, as well as differences in patterns of positive selection and levels of gene expression, also strongly depended on the specific histories of the three regions considered. Most strikingly, and unexpectedly, the allopolyploid species showed signs of hybridization with different diploid relatives or multiple origins in different parts of its range. Regardless if it was hybridization or multiple origins, this profoundly altered the relationship between the two subgenomes in different regions. Hence, our study illustrates how both the genomic structure and ecological arena interact to determine the evolutionary trajectories of allopolyploid species.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-379946 (URN)10.1371/journal.pgen.1007949 (DOI)000459970100033 ()30768594 (PubMedID)
Funder
Swedish Research Council, 2012-04999Swedish Research Council, 2015-03797
Note

De 2 första författarna delar förstaförfattarskapet.

Available from: 2019-03-25 Created: 2019-03-25 Last updated: 2019-03-25Bibliographically approved
Glemin, S., Scornavacca, C., Dainat, J., Burgarella, C., Viader, V., Ardisson, M., . . . Ranwez, V. (2019). Pervasive hybridizations in the history of wheat relatives. Science Advances, 5(5), Article ID eaav9188.
Open this publication in new window or tab >>Pervasive hybridizations in the history of wheat relatives
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2019 (English)In: Science Advances, E-ISSN 2375-2548, Vol. 5, no 5, article id eaav9188Article in journal (Refereed) Published
Abstract [en]

Cultivated wheats are derived from an intricate history of three genomes, A, B, and D, present in both diploid and polyploid species. It was recently proposed that the D genome originated from an ancient hybridization between the A and B lineages. However, this result has been questioned, and a robust phylogeny of wheat relatives is still lacking. Using transcriptome data from all diploid species and a new methodological approach, our comprehensive phylogenomic analysis revealed that more than half of the species descend from an ancient hybridization event but with a more complex scenario involving a different parent than previously thought-Aegilops mutica, an overlooked wild species-instead of the B genome. We also detected other extensive gene flow events that could explain long-standing controversies in the classification of wheat relatives.

Place, publisher, year, edition, pages
AMER ASSOC ADVANCEMENT SCIENCE, 2019
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-387971 (URN)10.1126/sciadv.aav9188 (DOI)000470125000086 ()31049399 (PubMedID)
Note

De två första författarna delar förstaförfattarskapet.

Available from: 2019-06-27 Created: 2019-06-27 Last updated: 2019-06-27Bibliographically approved
Kryvokhyzha, D., Milesi, P., Duan, T., Orsucci, M., Wright, S. I., Glemin, S. & Lascoux, M. (2019). Towards the new normal: Transcriptomic convergence and genomic legacy of the two subgenomes of an allopolyploid weed (Capsella bursa-pastoris). PLoS Genetics, 15(5), Article ID e1008131.
Open this publication in new window or tab >>Towards the new normal: Transcriptomic convergence and genomic legacy of the two subgenomes of an allopolyploid weed (Capsella bursa-pastoris)
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2019 (English)In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 15, no 5, article id e1008131Article in journal (Refereed) Published
Abstract [en]

Allopolyploidy has played a major role in plant evolution but its impact on genome diversity and expression patterns remains to be understood. Some studies found important genomic and transcriptomic changes in allopolyploids, whereas others detected a strong parental legacy and more subtle changes. The allotetraploid C. bursa-pastoris originated around 100,000 years ago and one could expect the genetic polymorphism of the two subgenomes to follow similar trajectories and their transcriptomes to start functioning together. To test this hypothesis, we sequenced the genomes and the transcriptomes (three tissues) of allotetraploid C. bursa-pastoris and its parental species, the outcrossing C. grandiflora and the self-fertilizing C. orientalis. Comparison of the divergence in expression between subgenomes, on the one hand, and divergence in expression between the parental species, on the other hand, indicated a strong parental legacy with a majority of genes exhibiting a conserved pattern and cis-regulation. However, a large proportion of the genes that were differentially expressed between the two subgenomes, were also under trans-regulation reflecting the establishment of a new regulatory pattern. Parental dominance varied among tissues: expression in flowers was closer to that of C. orientalis and expression in root and leaf to that of C. grandiflora. Since deleterious mutations accumulated preferentially on the C. orientalis subgenome, the bias in expression towards C. orientalis observed in flowers indicates that expression changes could be adaptive and related to the selfing syndrome, while biases in the roots and leaves towards the C. grandiflora subgenome may be reflective of the differential genetic load.

Place, publisher, year, edition, pages
PUBLIC LIBRARY SCIENCE, 2019
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-387963 (URN)10.1371/journal.pgen.1008131 (DOI)000470208000025 ()31083657 (PubMedID)
Funder
Swedish Research Council, 2015-03797
Available from: 2019-06-27 Created: 2019-06-27 Last updated: 2019-06-27Bibliographically approved
Galtier, N., Roux, C., Rousselle, M., Romiguier, J., Figuet, E., Glémin, S., . . . Duret, L. (2018). Codon Usage Bias in Animals: Disentangling the Effects of Natural Selection, Effective Population Size, and GC-Biased Gene Conversion. Molecular biology and evolution, 35(5), 1092-1103
Open this publication in new window or tab >>Codon Usage Bias in Animals: Disentangling the Effects of Natural Selection, Effective Population Size, and GC-Biased Gene Conversion
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2018 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, no 5, p. 1092-1103Article in journal (Refereed) Published
Abstract [en]

Selection on codon usage bias is well documented in a number of microorganisms. Whether codon usage is also generally shaped by natural selection in large organisms, despite their relatively small effective population size (Ne), is unclear. In animals, the population genetics of codon usage bias has only been studied in a handful of model organisms so far, and can be affected by confounding, nonadaptive processes such as GC-biased gene conversion and experimental artefacts. Using population transcriptomics data, we analyzed the relationship between codon usage, gene expression, allele frequency distribution, and recombination rate in 30 nonmodel species of animals, each from a different family, covering a wide range of effective population sizes. We disentangled the effects of translational selection and GC-biased gene conversion on codon usage by separately analyzing GC-conservative and GC-changing mutations. We report evidence for effective translational selection on codon usage in large-Ne species of animals, but not in small-Ne ones, in agreement with the nearly neutral theory of molecular evolution. C- and T-ending codons tend to be preferred over synonymous G- and A-ending ones, for reasons that remain to be determined. In contrast, we uncovered a conspicuous effect of GC-biased gene conversion, which is widespread in animals and the main force determining the fate of AT↔GC mutations. Intriguingly, the strength of its effect was uncorrelated with Ne.

Keywords
synonymous codon usage, GC-content, recombination, evolution, gene expression, nonmodel organisms
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-356513 (URN)10.1093/molbev/msy015 (DOI)000431889600005 ()29390090 (PubMedID)
Funder
EU, European Research Council, 232971
Available from: 2018-08-10 Created: 2018-08-10 Last updated: 2018-08-10Bibliographically approved
Mendoza, S. P., Lascoux, M. & Glemin, S. (2018). Competitive ability of Capsella species with different mating systems and ploidy levels. Annals of Botany, 121(6), 1257-1264
Open this publication in new window or tab >>Competitive ability of Capsella species with different mating systems and ploidy levels
2018 (English)In: Annals of Botany, ISSN 0305-7364, E-ISSN 1095-8290, Vol. 121, no 6, p. 1257-1264Article in journal (Refereed) Published
Abstract [en]

Background and Aims

Capsella is a model genus for studying the transition from outcrossing to selfing, with or without change in ploidy levels. The genomic consequences and changes in reproductive traits (selfing syndrome) associated with these shifts have been studied in depth. However, potential ecological divergence among species of the genus has not been determined. Among ecological traits, competitive ability could be relevant for selfing evolution, as selfing has been shown to be statistically associated with reduced competitiveness in a recent meta-analysis.

Methods

We assessed the effect of competition on three Capsella species differing in their mating system and ploidy level. We used an experimental design where fitness related traits were measured in focal individuals with and without competitors.

Key Results

The diploid selfer (C. rubella) was most sensitive to competition, whereas the tetraploid selfer (C. bursa-pastoris) performed the best, with the diploid outcrosser (C. grandiflora) being intermediate.

Conclusions

These results add to the detailed characterization of Capsella species and highlight the possible roles of ecological context and ploidy in the evolutionary trajectories of selfing species.

Keywords
Capsella, competition, mating system, outcrossing, ploidy, selfing
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-356872 (URN)10.1093/aob/mcy014 (DOI)000432059300017 ()29471370 (PubMedID)
Funder
Swedish Research Council
Available from: 2018-08-09 Created: 2018-08-09 Last updated: 2018-08-09Bibliographically approved
Sauvage, C., Rau, A., Aichholz, C., Chadoeuf, J., Sarah, G., Ruiz, M., . . . Glemin, S. (2017). Domestication rewired gene expression and nucleotide diversity patterns in tomato. The Plant Journal, 91(4), 631-645
Open this publication in new window or tab >>Domestication rewired gene expression and nucleotide diversity patterns in tomato
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2017 (English)In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 91, no 4, p. 631-645Article in journal (Refereed) Published
Abstract [en]

Plant domestication has led to considerable phenotypic modifications from wild species to modern varieties. However, although changes in key traits have been well documented, less is known about the underlying molecular mechanisms, such as the reduction of molecular diversity or global gene co-expression patterns. In this study, we used a combination of gene expression and population genetics in wild and crop tomato to decipher the footprints of domestication. We found a set of 1729 differentially expressed genes (DEG) between the two genetic groups, belonging to 17 clusters of co-expressed DEG, suggesting that domestication affected not only individual genes but also regulatory networks. Five co-expression clusters were enriched in functional terms involving carbohydrate metabolism or epigenetic regulation of gene expression. We detected differences in nucleotide diversity between the crop and wild groups specific to DEG. Our study provides an extensive profiling of the rewiring of gene co-expression induced by the domestication syndrome in one of the main crop species.

Place, publisher, year, edition, pages
WILEY, 2017
Keywords
domestication, gene co-expression, comparative genomics, selective sweep, tomato
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-333720 (URN)10.1111/tpj.13592 (DOI)000407011100006 ()28488328 (PubMedID)
Available from: 2017-11-16 Created: 2017-11-16 Last updated: 2017-11-16Bibliographically approved
Clement, Y., Sarah, G., Holtz, Y., Homa, F., Pointet, S., Contreras, S., . . . Glemin, S. (2017). Evolutionary forces affecting synonymous variations in plant genomes. PLoS Genetics, 13(5), Article ID e1006799.
Open this publication in new window or tab >>Evolutionary forces affecting synonymous variations in plant genomes
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2017 (English)In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 13, no 5, article id e1006799Article in journal (Refereed) Published
Abstract [en]

Base composition is highly variable among and within plant genomes, especially at third codon positions, ranging from GC-poor and homogeneous species to GC-rich and highly heterogeneous ones (particularly Monocots). Consequently, synonymous codon usage is biased in most species, even when base composition is relatively homogeneous. The causes of these variations are still under debate, with three main forces being possibly involved: mutational bias, selection and GC-biased gene conversion (gBGC). So far, both selection and gBGC have been detected in some species but how their relative strength varies among and within species remains unclear. Population genetics approaches allow to jointly estimating the intensity of selection, gBGC and mutational bias. We extended a recently developed method and applied it to a large population genomic dataset based on transcriptome sequencing of 11 angiosperm species spread across the phylogeny. We found that at synonymous positions, base composition is far from mutation-drift equilibrium in most genomes and that gBGC is a widespread and stronger process than selection. gBGC could strongly contribute to base composition variation among plant species, implying that it should be taken into account in plant genome analyses, especially for GC-rich ones.

Place, publisher, year, edition, pages
PUBLIC LIBRARY SCIENCE, 2017
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-328724 (URN)10.1371/journal.pgen.1006799 (DOI)000402884800045 ()28531201 (PubMedID)
Available from: 2017-08-30 Created: 2017-08-30 Last updated: 2017-08-30Bibliographically approved
Noel, E., Jarne, P., Glemin, S., MacKenzie, A., Segard, A., Sarda, V. & David, P. (2017). Experimental Evidence for the Negative Effects of Self-Fertilization on the Adaptive Potential of Populations. Current Biology, 27(2), 237-242
Open this publication in new window or tab >>Experimental Evidence for the Negative Effects of Self-Fertilization on the Adaptive Potential of Populations
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2017 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 27, no 2, p. 237-242Article in journal (Refereed) Published
Abstract [en]

Self-fertilization is widely believed to be an "evolutionary dead end" [1, 2], increasing the risk of extinction [3] and the accumulation of deleterious mutations in genomes [4]. Strikingly, while the failure to adapt has always been central to the dead-end hypothesis [1, 2], there are no quantitative genetic selection experiments comparing the response to positive selection in selfing versus outcrossing populations. Here we studied the response to selection on a morphological trait in laboratory populations of a hermaphroditic, self fertile snail under either selfing or outcrossing. We applied both treatments to two types of populations: some having undergone frequent selfing and purged a substantial fraction of their mutation load in their recent history [5], and others continuously maintained under outcrossing. Populations with a history of outcrossing respond faster to selection than those that have experienced selfing. In addition, when self-fertilization occurs during selection, the response is initially fast but then rapidly slows, while outcrossing populations maintain their response throughout the experiment. This occurs irrespective of past selfing history, suggesting that high levels of inbreeding depression, contrary to expectation [6], do not set strong limits to the response to selection under inbreeding, at least at the timescale of a few generations. More surprisingly, phenotypic variance is consistently higher under selfing, although it quickly becomes less responsive to selection. This implies an increase in non-heritable variance, hence a breakdown of developmental canalization [7] under selfing. Our findings provide the first empirical support of the short-term positive and long-term negative effects of selfing on adaptive potential.

National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-317610 (URN)10.1016/j.cub.2016.11.015 (DOI)000392904000024 ()28041795 (PubMedID)
Available from: 2017-03-16 Created: 2017-03-16 Last updated: 2017-11-29Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0001-7260-4573

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