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Glemin, S.

Publications and source records attributed to Glemin, S..

7 recordsLinked to original sources

Dioecy in plants: an evolutionary dead end? Insights from a population genomics study in the Silene genus

About 15,000 angiosperm species ([~]6%) have separate sexes, a phenomenon known as dioecy. Early work reported a lower species richness in dioecious compared to non-dioecious sister clades, which was taken to suggest that dioecy might be an evolutionary dead end. More recently, phylogenetic analyses using different methodologies have challenged this conclusion. Here, we used a population genomics approach to look for evidence of evolutionary handicaps of dioecy in the Silene genus at the molecular level. We obtained RNA-seq data of individuals from several populations in 13 closely related species with different breeding systems: seven dioecious, three hermaphroditic and three gynodioecious species. We show that dioecy is associated with increased genetic diversity and a higher selection efficacy both against deleterious and for beneficial mutations while controlling for differences in population size. We conclude that, in the Silene genus, dioecious species bear no sign of mutational burden or upcoming extinction. On the contrary, dioecious species harbor a higher potential for adaptation than their non-dioecious relatives. Our results do not support the evolutionary dead end hypothesis and re-open the question why dioecy is rare in angiosperms.\n\nSignificance statementDioecy (=separate sexes) is much rarer in flowering plants compared to animals and other organisms. The \"dead-end hypothesis\" states that dioecious plant populations might experience evolutionary handicaps such as low seed dispersal (as only 50% of the individuals, the females, contribute), which might cause high genetic drift, low adaptation and ultimately extinction. Here we tested this hypothesis by focusing on the genus Silene and by comparing the population genetics of 13 dioecious and non-dioecious species. We found that dioecious Silene species exhibit lower genetic drift and more adaptation compared to their non-dioecious relatives. Our results thus reject the dead-end hypothesis and re-open the question of why dioecy is rare in flowering plants.

evolutionary biology

Local adaptation and maladaptation during the worldwide range expansion of a self-fertilizing plant

Species having experienced rapid range expansion represent unique opportunities to evaluate the dynamics of adaptation during colonization of new environments. We investigated the consequences of range expansion on local adaptation of a successful worldwide colonizer, the shepherds purse Capsella bursa-pastoris. This species is an annual weed that originated recently in Eurasia and has now broadly colonized both temperate and subtropical areas. We assessed the performance, genetic diversity, and phenology of field-collected accessions belonging to three distinct genetic clusters of decreasing age (Middle East, Europe and Asia) in three common gardens in Europe, Asia and North America. To understand the genetic basis of local adaptation in this species, we also tested for correlation between SNP allele frequencies and environmental factors in Europe and Asia. Overall, we showed that patterns of local adaptation depended on population history: some older populations were weakly adapted to local conditions while those closer to the front of the colonization wave, far from the origin of the species, were maladapted whatever the common gardens. Altogether, our results have important consequences for the understanding of the evolution and adaptation of self-fertilizing plant during range expansion.

evolutionary biology

Pervasive hybridizations in the history of wheat relatives

Bread wheat and durum wheat derive from an intricate evolutionary history of three genomes, namely A, B and D, present in both extent diploid and polyploid species. Despite its importance for wheat research, no consensus on the phylogeny of the wheat clade has emerged so far, possibly because of hybridizations and gene flows that make phylogeny reconstruction challenging. Recently, it has been proposed that the D genome originated from an ancient hybridization event between the A and B genomes1. However, the study only relied on four diploid wheat relatives when 13 species are accessible. Using transcriptome data from all diploid species and a new methodological approach, we provide the first comprehensive phylogenomic analysis of this group. Our analysis reveals that most species belong to the D-genome lineage and descend from the previously detected hybridization event, but with a more complex scenario and with a different parent than previously thought. If we confirmed that one parent was the A genome, we found that the second was not the B genome but the ancestor of Aegilops mutica (T genome), an overlooked wild species. We also unravel evidence of other massive gene flow events that could explain long-standing controversies in the classification of wheat relatives. We anticipate that these results will strongly affect future wheat research by providing a robust evolutionary framework and refocusing interest on understudied species. The new method we proposed should also be pivotal for further methodological developments to reconstruct species relationship with multiple hybridizations.

evolutionary biology

Parental legacy, demography, and introgression influenced the evolution of the two subgenomes of the tetraploid Capsella bursa-pastoris (Brassicaceae)

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 and 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 (Cg) and the other one from the selfing and genetically depauperate Capsella orientalis (Co). For each subgenome, we assessed its relationship with the diploid relatives, temporal change of effective population size Ne, signatures of positive and negative selection, and gene expression patterns. Introgression between C. bursa-pastoris and its diploid relatives was widespread and the two subgenomes were impacted differentially depending on geographic region. In all three regions, Ne of the two subgenomes decreased gradually and the Co subgenome accumulated more deleterious changes than Cg. Selective sweeps were more common on the Cg subgenome in Europe and the Middle East, and on the Co subgenome in Asia. In contrast, differences in expression were limited with the Cg subgenome slightly more expressed than 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 and were differentially affected by introgression and selection.

evolutionary biology

Competitive ability of a tetraploid selfing species (Capsella bursa-pastoris) across its expansion range and comparison with its sister species

Self-fertilization is often associated with ecological traits corresponding to the ruderal strategy in Grimes Competitive-Stress-tolerant-Ruderal (CSR) classification of ecological strategies. Consequently, selfers are expected to be less competitive than outcrossers, either because of a colonization/competition trade-off or because of the deleterious genetic effects of selfing. Range expansion could reduce further competitive ability while polyploidy could mitigate the effects of selfing. Although suggested by meta-analyses, these predictions have not been directly tested yet. We compared the competitive ability of four Capsella species differing by their mating system and ploidy level. We found that the two diploid selfing species (C. rubella and C. orientalis) were more sensitive to competition than the diploid outcrosser (C. grandiflora), and that the tetraploid selfer (C. bursa-pastoris) was intermediate. Within C. bursa-pastoris, we also found that sensitivity to competition increased in parallel to range expansion. These results highlight the possible roles of ecological context and ploidy in the evolutionary trajectories of selfing species.

evolutionary biology

Codon usage bias in animals: disentangling the effects of natural selection, effective population size and GC-biased gene conversion

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. Codon usage bias in animals has only been studied in a handful of model organisms so far, and can be affected by confounding, non-adaptive processes such as GC-biased gene conversion and experimental artefacts. Using population transcriptomics data we analysed the relationship between codon usage, gene expression, allele frequency distribution and recombination rate in 31 non-model 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 analysing 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 are generally 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{leftrightarrow}GC mutations. Intriguingly, the strength of its effect was uncorrelated with Ne.

evolutionary biology

Evolutionary forces affecting synonymous variations in plant genomes

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 datasets based on transcriptome sequencing of 11 angiosperm species spread across the phylogeny. We found that 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.

evolutionary biology