Polygenic selection to a changing optimum under self-fertilisation.

Many traits are polygenic, affected by multiple genetic variants throughout the genome. Selection acting on these traits involves co-ordinated allele-frequency changes at these underlying variants, and this process has been extensively studied in random-mating populations. Yet many species self-fertilise to some degree, which incurs changes to genetic diversity, recombination and genome segregation. These factors cumulatively influence how polygenic selection is realised in nature. Here, we use analytical modelling and stochastic simulations to investigate to what extent self-fertilisation affects polygenic adaptation to a new environment. Our analytical solutions show that while selfing can increase adaptation to an optimum, it incurs linkage disequilibrium that can slow down the initial spread of favoured mutations due to selection interference, and favours the fixation of alleles with opposing trait effects. Simulations show that while selection interference is present, high levels of selfing (at least 90%) aids adaptation to a new optimum, showing a higher long-term fitness. If mutations are pleiotropic then only a few major-effect variants fix along with many neutral hitchhikers, with a transient increase in linkage disequilibrium. These results show potential advantages to self-fertilisation when adapting to a new environment, and how the mating system affects the genetic composition of polygenic selection.

Diversity in Recombination Hotspot Characteristics and Gene Structure Shape Fine-Scale Recombination Patterns in Plant Genomes.

During the meiosis of many eukaryote species, crossovers tend to occur within narrow regions called recombination hotspots. In plants, it is generally thought that gene regulatory sequences, especially promoters and 5' to 3' untranslated regions, are enriched in hotspots, but this has been characterized in a handful of species only. We also lack a clear description of fine-scale variation in recombination rates within genic regions and little is known about hotspot position and intensity in plants. To address this question, we constructed fine-scale recombination maps from genetic polymorphism data and inferred recombination hotspots in 11 plant species. We detected gradients of recombination in genic regions in most species, yet gradients varied in intensity and shape depending on specific hotspot locations and gene structure. To further characterize recombination gradients, we decomposed them according to gene structure by rank and number of exons. We generalized the previously observed pattern that recombination hotspots are organized around the boundaries of coding sequences, especially 5' promoters. However, our results also provided new insight into the relative importance of the 3' end of genes in some species and the possible location of hotspots away from genic regions in some species. Variation among species seemed driven more by hotspot location among and within genes than by differences in size or intensity among species. Our results shed light on the variation in recombination rates at a very fine scale, revealing the diversity and complexity of genic recombination gradients emerging from the interaction between hotspot location and gene structure.

Diversity and determinants of recombination landscapes in flowering plants.

During meiosis, crossover rates are not randomly distributed along the chromosome and their location may have a strong impact on the functioning and evolution of the genome. To date, the broad diversity of recombination landscapes among plants has rarely been investigated and a formal comparative genomic approach is still needed to characterize and assess the determinants of recombination landscapes among species and chromosomes. We gathered genetic maps and genomes for 57 flowering plant species, corresponding to 665 chromosomes, for which we estimated large-scale recombination landscapes. We found that the number of crossover per chromosome spans a limited range (between one to five/six) whatever the genome size, and that there is no single relationship across species between genetic map length and chromosome size. Instead, we found a general relationship between the relative size of chromosomes and recombination rate, while the absolute length constrains the basal recombination rate for each species. At the chromosome level, we identified two main patterns (with a few exceptions) and we proposed a conceptual model explaining the broad-scale distribution of crossovers where both telomeres and centromeres play a role. These patterns correspond globally to the underlying gene distribution, which affects how efficiently genes are shuffled at meiosis. These results raised new questions not only on the evolution of recombination rates but also on their distribution along chromosomes.

Mating system and speciation I: Accumulation of genetic incompatibilities in allopatry.

Self-fertilisation is widespread among hermaphroditic species across the tree of life. Selfing has many consequences on the genetic diversity and the evolutionary dynamics of populations, which may in turn affect macroevolutionary processes such as speciation. On the one hand, because selfing increases genetic drift and reduces migration rate among populations, it may be expected to promote speciation. On the other hand, because selfing reduces the efficacy of selection, it may be expected to hamper ecological speciation. To better understand under which conditions and in which direction selfing affects the build-up of reproductive isolation, an explicit population genetics model is required. Here, we focus on the interplay between genetic drift, selection and genetic linkage by studying speciation without gene flow. We test how fast populations with different rates of selfing accumulate mutations leading to genetic incompatibilities. When speciation requires populations to pass through a fitness valley caused by underdominant and compensatory mutations, selfing reduces the depth and/or breadth of the valley, and thus overall facilitates the fixation of incompatibilities. When speciation does not require populations to pass through a fitness valley, as for Bateson-Dobzhanzky-Muller incompatibilities (BDMi), the lower effective population size and higher genetic linkage in selfing populations both facilitate the fixation of incompatibilities. Interestingly, and contrary to intuitive expectations, local adaptation does not always accelerate the fixation of incompatibilities in outcrossing relative to selfing populations. Our work helps to clarify how incompatibilities accumulate in selfing vs. outcrossing lineages, and has repercussions on the pace of speciation as well as on the genetic architecture of reproductive isolation.

Trait-dependent diversification in angiosperms: Patterns, models and data.

Variation in species richness across the tree of life, accompanied by the incredible variety of ecological and morphological characteristics found in nature, has inspired many studies to link traits with species diversification. Angiosperms are a highly diverse group that has fundamentally shaped life on earth since the Cretaceous, and illustrate how species diversification affects ecosystem functioning. Numerous traits and processes have been linked to differences in species richness within this group, but we know little about their relative importance and how they interact. Here, we synthesised data from 152 studies that used state-dependent speciation and extinction (SSE) models on angiosperm clades. Intrinsic traits related to reproduction and morphology were often linked to diversification but a set of universal drivers did not emerge as traits did not have consistent effects across clades. Importantly, SSE model results were correlated to data set properties - trees that were larger, older or less well-sampled tended to yield trait-dependent outcomes. We compared these properties to recommendations for SSE model use and provide a set of best practices to follow when designing studies and reporting results. Finally, we argue that SSE model inferences should be considered in a larger context incorporating species' ecology, demography and genetics.

Expression pattern of resynthesized allotetraploid Capsella is determined by hybridization, not whole-genome duplication.

Polyploidization, the process leading to the increase in chromosome sets, is a major evolutionary transition in plants. Whole-genome duplication (WGD) within the same species gives rise to autopolyploids, whereas allopolyploids result from a compound process with two distinct components: WGD and interspecific hybridization. To dissect the instant effects of WGD and hybridization on gene expression and phenotype, we created a series of synthetic hybrid and polyploid Capsella plants, including diploid hybrids, autotetraploids of both parental species, and two kinds of resynthesized allotetraploids with different orders of WGD and hybridization. Hybridization played a major role in shaping the relative expression pattern of the neo-allopolyploids, whereas WGD had almost no immediate effect on relative gene expression pattern but, nonetheless, still affected phenotypes. No transposable element-mediated genomic shock scenario was observed in either neo-hybrids or neo-polyploids. Finally, WGD and hybridization interacted and the distorting effects of WGD were less strong in hybrids. Whole-genome duplication may even improve hybrid fertility. In summary, while the initial relative gene expression pattern in neo-allotetraploids was almost entirely determined by hybridization, WGD only had trivial effects on relative expression patterns, both processes interacted and had a strong impact on physical attributes and meiotic behaviors.

Pulled Diversification Rates, Lineages-Through-Time Plots, and Modern Macroevolutionary Modeling.

Estimating time-dependent rates of speciation and extinction from dated phylogenetic trees of extant species (timetrees), and determining how and why they vary, is key to understanding how ecological and evolutionary processes shape biodiversity. Due to an increasing availability of phylogenetic trees, a growing number of process-based methods relying on the birth-death model have been developed in the last decade to address a variety of questions in macroevolution. However, this methodological progress has regularly been criticized such that one may wonder how reliable the estimations of speciation and extinction rates are. In particular, using lineages-through-time (LTT) plots, a recent study has shown that there are an infinite number of equally likely diversification scenarios that can generate any timetree. This has led to questioning whether or not diversification rates should be estimated at all. Here, we summarize, clarify, and highlight technical considerations on recent findings regarding the capacity of models to disentangle diversification histories. Using simulations, we illustrate the characteristics of newly proposed "pulled rates" and their utility. We recognize that the recent findings are a step forward in understanding the behavior of macroevolutionary modeling, but they in no way suggest we should abandon diversification modeling altogether. On the contrary, the study of macroevolution using phylogenetic trees has never been more exciting and promising than today. We still face important limitations in regard to data availability and methods, but by acknowledging them we can better target our joint efforts as a scientific community. [Birth-death models; extinction; phylogenetics; speciation.].

Dioecy Is Associated with High Genetic Diversity and Adaptation Rates in the Plant Genus Silene.

About 15,000 angiosperm species (∼6%) have separate sexes, a phenomenon known as dioecy. Why dioecious taxa are so rare is still an open question. Early work reported lower species richness in dioecious compared with nondioecious sister clades, raising the hypothesis that dioecy may be an evolutionary dead-end. This hypothesis has been recently challenged by macroevolutionary analyses that detected no or even positive effect of dioecy on diversification. However, the possible genetic consequences of dioecy at the population level, which could drive the long-term fate of dioecious lineages, have not been tested so far. Here, we used a population genomics approach in the Silene genus to look for possible effects of dioecy, especially for potential evidence of evolutionary handicaps of dioecy underlying the dead-end hypothesis. We collected individual-based RNA-seq data from several populations in 13 closely related species with different sexual systems: seven dioecious, three hermaphroditic, and three gynodioecious species. We show that dioecy is associated with increased genetic diversity, as well as higher selection efficacy both against deleterious mutations and for beneficial mutations. The results hold after controlling for phylogenetic inertia, differences in species census population sizes and geographic ranges. We conclude that dioecious Silene species neither show signs of increased mutational load nor genetic evidence for extinction risk. We discuss these observations in the light of the possible demographic differences between dioecious and self-compatible hermaphroditic species and how this could be related to alternatives to the dead-end hypothesis to explain the rarity of dioecy.

What does the distribution of fitness effects of new mutations reflect? Insights from plants.

The distribution of fitness effects (DFE) of new mutations plays a central role in molecular evolution. It is therefore crucial to be able to estimate it accurately from genomic data and to understand the factors that shape it. After a rapid overview of available methods to characterize the fitness effects of mutations, we review what is known on the factors affecting them in plants. Available data indicate that life history traits (e.g. mating system and longevity) have a major effect on the DFE. By contrast, the impact of demography within species appears to be more limited. These results remain to be confirmed, and methods to estimate the joint evolution of demography, life history traits, and the DFE need to be developed.

How broad is the selfing syndrome? Insights from convergent evolution of gene expression across species and tissues in the Capsella genus.

The shift from outcrossing to selfing is one of the main evolutionary transitions in plants. It is accompanied by profound effects on reproductive traits, the so-called selfing syndrome. Because the transition to selfing also implies deep genomic and ecological changes, one also expects to observe a genomic selfing syndrome. We took advantage of the three independent transitions from outcrossing to selfing in the Capsella genus to characterize the overall impact of mating system change on RNA expression, in flowers but also in leaves and roots. We quantified the extent of both selfing and genomic syndromes, and tested whether changes in expression corresponded to adaptation to selfing or to relaxed selection on traits that were constrained in outcrossers. Mating system change affected gene expression in all three tissues but more so in flowers than in roots and leaves. Gene expression in selfing species tended to converge in flowers but diverged in the two other tissues. Hence, convergent adaptation to selfing dominates in flowers, whereas genetic drift plays a more important role in leaves and roots. The effect of mating system transition is not limited to reproductive tissues and corresponds to both adaptation to selfing and relaxed selection on previously constrained traits.

Competitive ability depends on mating system and ploidy level across Capsella species.

BACKGROUND AND AIMS: Self-fertilization is often associated with ecological traits corresponding to the ruderal strategy, and 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. If pollinators are not limited, individual fitness is thus expected to be higher in outcrossers than in selfers and, within selfers, in polyploids than in diploids. Although often proposed in the botanical literature and also suggested by meta-analyses, these predictions have not been directly tested yet. METHODS: In order to compare fitness and the competitive ability of four Capsella species with a different mating system and ploidy level, we combined two complementary experiments. First, we carried out an experiment outdoors in north-west Greece, i.e. within the range of the obligate outcrossing species, C. grandiflora, where several life history traits were measured under two different disturbance treatments, weeded plots vs. unweeded plots. To better control competition and to remove potential effects of local adaptation of the outcrosser, we also performed a similar competition experiment but under growth chamber conditions. KEY RESULTS: In the outdoor experiment, disturbance of the environment did not affect the phenotype in any of the four species. For most traits, the obligate outcrossing species performed better than all selfing species. In contrast, polyploids did not survive or reproduce better than diploids. Under controlled conditions, as in the field experiment, the outcrosser had a higher fitness than selfing species and was less affected by competition. Finally, contrary to the outdoor experiment where the two behaved identically, polyploid selfers were less affected by competition than diploid selfes. CONCLUSIONS: In the Capsella genus, selfing induces lower fitness than outcrossing and can also reduce competitive ability. The effect of polyploidy is, however, unclear. These results highlight the possible roles of ecological context in the evolution of selfing species.

Towards the new normal: Transcriptomic convergence and genomic legacy of the two subgenomes of an allopolyploid weed (Capsella bursa-pastoris).

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.

Parental legacy, demography, and admixture 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 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 (CbpCg) and the other one from the selfing and genetically depauperate Capsella orientalis (CbpCo). For each subgenome, we assessed its relationship with the diploid relatives, temporal changes of effective population size (Ne), signatures of positive and negative selection, and gene expression patterns. In all three regions, Ne of the two subgenomes decreased gradually over time and the CbpCo subgenome accumulated more deleterious changes than CbpCg. 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 CbpCg subgenome in Europe and the Middle East, and on the CbpCo subgenome in Asia. In contrast, differences in expression were limited with the CbpCg subgenome slightly more expressed than CbpCo 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.

The ecology of the genome and the dynamics of the biological dark matter.

Transposable elements (TEs) are essential components of the eukaryotic genomes. While mostly deleterious, evidence is mounting that TEs provide the host with beneficial adaptations. How 'selfish' or 'parasitic' DNA persists until it helps species evolution is emerging as a major evolutionary puzzle, especially in asexual taxa where the lack of sex strongly impede the spread of TEs. Since occasional but unchecked TE proliferations would ultimately drive host lineages toward extinction, asexual genomes are typically predicted to be free of TEs, which contrasts with their persistence in asexual taxa. We designed innovative 'Eco-genomic' models that account for both host demography and within-host molecular mechanisms of transposition and silencing to analyze their impact on TE dynamics in asexual genome populations. We unraveled that the spread of TEs can be limited to a stable level by density-dependent purifying selection when TE copies are over-dispersed among lineages and the host demographic turn-over is fast. We also showed that TE silencing can protect host populations in two ways; by preventing TEs with weak effects to accumulate or by favoring the elimination of TEs with large effects. Our predictions may explain TE persistence in known asexual taxa that typically show fast demography and where TE copy number variation between lineages is expected. Such TE persistence in asexual taxa potentially has important implications for their evolvability and the preservation of sexual reproduction.

Analysis of diversity-dependent species evolution using concepts in population genetics.

In this work, we consider a two-type species model with trait-dependent speciation, extinction and transition rates under an evolutionary time scale. The scaling approach and the diffusion approximation techniques which are widely used in mathematical population genetics provide modeling tools and conceptual background to assist in the study of species dynamics, and help exploring the analogy between trait-dependent species diversification and the evolution of allele frequencies in the population genetics setting. The analytical framework specified is then applied to models incorporating diversity-dependence, in order to infer effective results from processes in which the net diversification of species depends on the total number of species. In particular, the long term fate of a rare trait may be analyzed under a partly symmetric scenario, using a time-change transform technique.

Evolutionary transcriptomics reveals the origins of olives and the genomic changes associated with their domestication.

The olive (Olea europaea L. subsp. europaea) is one of the oldest and most socio-economically important cultivated perennial crop in the Mediterranean region. Yet, its origins are still under debate and the genetic bases of the phenotypic changes associated with its domestication are unknown. We generated RNA-sequencing data for 68 wild and cultivated olive trees to study the genetic diversity and structure both at the transcription and sequence levels. To localize putative genes or expression pathways targeted by artificial selection during domestication, we employed a two-step approach in which we identified differentially expressed genes and screened the transcriptome for signatures of selection. Our analyses support a major domestication event in the eastern part of the Mediterranean basin followed by dispersion towards the West and subsequent admixture with western wild olives. While we found large changes in gene expression when comparing cultivated and wild olives, we found no major signature of selection on coding variants and weak signals primarily affected transcription factors. Our results indicated that the domestication of olives resulted in only moderate genomic consequences and that the domestication syndrome is mainly related to changes in gene expression, consistent with its evolutionary history and life history traits.

The Evolutionary Interplay between Adaptation and Self-Fertilization.

Genome-wide surveys of nucleotide polymorphisms, obtained from next-generation sequencing, have uncovered numerous examples of adaptation in self-fertilizing organisms, especially regarding changes to climate, geography, and reproductive systems. Yet existing models for inferring attributes of adaptive mutations often assume idealized outcrossing populations, which risks mischaracterizing properties of these variants. Recent theoretical work is emphasizing how various aspects of self-fertilization affects adaptation, yet empirical data on these properties are lacking. We review theoretical and empirical studies demonstrating how self-fertilization alters the process of adaptation, illustrated using examples from current sequencing projects. We propose ideas for how future research can more accurately quantify aspects of adaptation in self-fertilizers, including incorporating the effects of standing variation, demographic history, and polygenic adaptation.

Shift in ecological strategy helps marginal populations of shepherd's purse (Capsella bursa-pastoris) to overcome a high genetic load.

The outcome of species range expansion depends on the interplay of demographic, environmental and genetic factors. Self-fertilizing species usually show a higher invasive ability than outcrossers but selfing and bottlenecks during colonization also lead to an increased genetic load. The relationship between genomic and phenotypic characteristics of expanding populations has, hitherto, rarely been tested experimentally. We analysed how accessions of the shepherd's purse, Capsella bursa-pastoris, from the colonization front or from the core of the natural range performed under increasing density of competitors. First, accessions from the front showed a lower fitness than those from the core. Second, for all accessions, competitor density impacted negatively both vegetative growth and fruit production. However, despite their higher genetic load and lower absolute performances, accessions from the front were less affected by competition than accessions from the core. This seems to be due to phenotypic trade-offs and a shift in phenology that allow accessions from the front to avoid competition.

Evolution of putative barrier loci at an intermediate stage of speciation with gene flow in campions (Silene).

Understanding the origin of new species is a central goal in evolutionary biology. Diverging lineages often evolve highly heterogeneous patterns of genetic differentiation; however, the underlying mechanisms are not well understood. We investigated evolutionary processes governing genetic differentiation between the hybridizing campions Silene dioica (L.) Clairv. and S. latifolia Poiret. Demographic modelling indicated that the two species diverged with gene flow. The best-supported scenario with heterogeneity in both migration rate and effective population size suggested that a small proportion of the loci evolved without gene flow. Differentiation (F ST ) and sequence divergence (d XY ) were correlated and both tended to peak in the middle of most linkage groups, consistent with reduced gene flow at highly differentiated loci. Highly differentiated loci further exhibited signatures of selection. In between-species population pairs, isolation by distance was stronger for genomic regions with low between-species differentiation than for highly differentiated regions that may contain barrier loci. Moreover, differentiation landscapes within and between species were only weakly correlated, suggesting that linked selection due to shared recombination and gene density landscapes is not the dominant determinant of genetic differentiation in these lineages. Instead, our results suggest that divergent selection shaped the genomic landscape of differentiation between the two Silene species, consistent with predictions for speciation in the face of gene flow.

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 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.