Complex Polyploids: Origins, Genomic Composition, and Role of Introgressed Alleles.

Introgression allows polyploid species to acquire new genomic content from diploid progenitors or from other unrelated diploid or polyploid lineages, contributing to genetic diversity and facilitating adaptive allele discovery. In some cases, high levels of introgression elicit the replacement of large numbers of alleles inherited from the polyploid's ancestral species, profoundly reshaping the polyploid's genomic composition. In such complex polyploids it is often difficult to determine which taxa were the progenitor species and which taxa provided additional introgressive blocks through subsequent hybridization. Here, we use population-level genomic data to reconstruct the phylogenetic history of Betula pubescens (downy birch), a tetraploid species often assumed to be of allopolyploid origin and which is known to hybridize with at least four other birch species. This was achieved by modeling of polyploidization and introgression events under the multispecies coalescent and then using an approximate Bayesian computation (ABC) rejection algorithm to evaluate and compare competing polyploidization models. We provide evidence that B. pubescens is the outcome of an autoploid genome doubling event in the common ancestor of B. pendula and its extant sister species, B. platyphylla, that took place approximately 178,000-188,000 generations ago. Extensive hybridization with B. pendula, B. nana, and B. humilis followed in the aftermath of autopolyploidization, with the relative contribution of each of these species to the B. pubescens genome varying markedly across the species' range. Functional analysis of B. pubescens loci containing alleles introgressed from B. nana identified multiple genes involved in climate adaptation, while loci containing alleles derived from B. humilis revealed several genes involved in the regulation of meiotic stability and pollen viability in plant species.

Between but Not Within-Species Variation in the Distribution of Fitness Effects.

New mutations provide the raw material for evolution and adaptation. The distribution of fitness effects (DFE) describes the spectrum of effects of new mutations that can occur along a genome, and is, therefore, of vital interest in evolutionary biology. Recent work has uncovered striking similarities in the DFE between closely related species, prompting us to ask whether there is variation in the DFE among populations of the same species, or among species with different degrees of divergence, that is whether there is variation in the DFE at different levels of evolution. Using exome capture data from six tree species sampled across Europe we characterized the DFE for multiple species, and for each species, multiple populations, and investigated the factors potentially influencing the DFE, such as demography, population divergence, and genetic background. We find statistical support for the presence of variation in the DFE at the species level, even among relatively closely related species. However, we find very little difference at the population level, suggesting that differences in the DFE are primarily driven by deep features of species biology, and those evolutionarily recent events, such as demographic changes and local adaptation, have little impact.

Hybridization mediated range expansion and climate change resilience in two keystone tree species of boreal forests.

Current global climate change is expected to affect biodiversity negatively at all scales leading to mass biodiversity loss. Many studies have shown that the distribution of allele frequencies across a species' range is often influenced by specific genetic loci associated with local environmental variables. This association reflects local adaptation and allele changes at those loci could thereby contribute to the evolutionary response to climate change. However, predicting how species will adapt to climate change from this type of data alone remains challenging. In the present study, we combined exome capture sequences and environmental niche reconstruction, to test multiple methods for assessing local adaptation and climate resilience in two widely distributed conifers, Norway spruce and Siberian spruce. Both species are keystone species of the boreal forest and share a vast hybrid zone. We show that local adaptation in conifers can be detected through allele frequency variation, population-level ecological preferences, and historical niche movement. Moreover, we integrated genetic and ecological information into genetic offset predictive models to show that hybridization plays a central role in expanding the niche breadth of the two conifer species and may help both species to cope better with future changing climates. This joint genetic and ecological analysis also identified spruce populations that are at risk under current climate change.

Phylogenetic Analysis of Allotetraploid Species Using Polarized Genomic Sequences.

Phylogenetic analysis of polyploid hybrid species has long posed a formidable challenge as it requires the ability to distinguish between alleles of different ancestral origins in order to disentangle their individual evolutionary history. This problem has been previously addressed by conceiving phylogenies as reticulate networks, using a two-step phasing strategy that first identifies and segregates homoeologous loci and then, during a second phasing step, assigns each gene copy to one of the subgenomes of an allopolyploid species. Here, we propose an alternative approach, one that preserves the core idea behind phasing-to produce separate nucleotide sequences that capture the reticulate evolutionary history of a polyploid-while vastly simplifying its implementation by reducing a complex multistage procedure to a single phasing step. While most current methods used for phylogenetic reconstruction of polyploid species require sequencing reads to be pre-phased using experimental or computational methods-usually an expensive, complex, and/or time-consuming endeavor-phasing executed using our algorithm is performed directly on the multiple-sequence alignment (MSA), a key change that allows for the simultaneous segregation and sorting of gene copies. We introduce the concept of genomic polarization that, when applied to an allopolyploid species, produces nucleotide sequences that capture the fraction of a polyploid genome that deviates from that of a reference sequence, usually one of the other species present in the MSA. We show that if the reference sequence is one of the parental species, the polarized polyploid sequence has a close resemblance (high pairwise sequence identity) to the second parental species. This knowledge is harnessed to build a new heuristic algorithm where, by replacing the allopolyploid genomic sequence in the MSA by its polarized version, it is possible to identify the phylogenetic position of the polyploid's ancestral parents in an iterative process. The proposed methodology can be used with long-read and short-read high-throughput sequencing data and requires only one representative individual for each species to be included in the phylogenetic analysis. In its current form, it can be used in the analysis of phylogenies containing tetraploid and diploid species. We test the newly developed method extensively using simulated data in order to evaluate its accuracy. We show empirically that the use of polarized genomic sequences allows for the correct identification of both parental species of an allotetraploid with up to 97% certainty in phylogenies with moderate levels of incomplete lineage sorting (ILS) and 87% in phylogenies containing high levels of ILS. We then apply the polarization protocol to reconstruct the reticulate histories of Arabidopsis kamchatica and Arabidopsis suecica, two allopolyploids whose ancestry has been well documented. [Allopolyploidy; Arabidopsis; genomic polarization; homoeologs; incomplete lineage sorting; phasing; polyploid phylogenetics; reticulate evolution.].

Despite structural identity, ace-1 heterogenous duplication resistance alleles are quite diverse in Anopheles mosquitoes.

Anopheles gambiae s.l. has been the target of intense insecticide treatment since the mid-20th century to try and control malaria. A substitution in the ace-1 locus has been rapidly selected for, allowing resistance to organophosphate and carbamate insecticides. Since then, two types of duplication of the ace-1 locus have been found in An. gambiae s.l. populations: homogeneous duplications that are composed of several resistance copies, or heterogeneous duplications that contain both resistance and susceptible copies. The substitution induces a trade-off between resistance in the presence of insecticides and disadvantages in their absence: the heterogeneous duplications allow the fixation of the intermediate heterozygote phenotype. So far, a single heterogeneous duplication has been described in An. gambiae s.l. populations (in contrast with the multiple duplicated alleles found in Culex pipiens mosquitoes). We used a new approach, combining long and short-read sequencing with Sanger sequencing to precisely identify and describe at least nine different heterogeneous duplications, in two populations of An. gambiae s.l. We show that these alleles share the same structure as the previously identified heterogeneous and homogeneous duplications, namely 203-kb tandem amplifications with conserved breakpoints. Our study sheds new light on the origin and maintenance of these alleles in An. gambiae s.l. populations, and their role in mosquito adaptation.

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.

Teasing apart the joint effect of demography and natural selection in the birth of a contact zone.

Vast population movements induced by recurrent climatic cycles have shaped the genetic structure of plant species. During glacial periods species were confined to low-latitude refugia from which they recolonized higher latitudes as the climate improved. This multipronged recolonization led to many lineages that later met and formed large contact zones. We utilize genomic data from 5000 Picea abies trees to test for the presence of natural selection during recolonization and establishment of a contact zone in Scandinavia. Scandinavian P. abies is today made up of a southern genetic cluster originating from the Baltics, and a northern one originating from Northern Russia. The contact zone delineating them closely matches the limit between two major climatic regions. We show that natural selection contributed to its establishment and maintenance. First, an isolation-with-migration model with genome-wide linked selection fits the data better than a purely neutral one. Second, many loci show signatures of selection or are associated with environmental variables. These loci, regrouped in clusters on chromosomes, are often related to phenology. Altogether, our results illustrate how climatic cycles, recolonization and selection can establish strong local adaptation along contact zones and affect the genetic architecture of adaptive traits.

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.

Killing two enemies with one stone? Genomics of resistance to two sympatric pathogens in Norway spruce.

Trees must cope with the attack of multiple pathogens, often simultaneously during their long lifespan. Ironically, the genetic and molecular mechanisms controlling this process are poorly understood. The objective of this study was to compare the genetic component of resistance in Norway spruce to Heterobasidion annosum s.s. and its sympatric congener Heterobasidion parviporum. Heterobasidion root- and stem-rot is a major disease of Norway spruce caused by members of the Heterobasidion annosum species complex. Resistance to both pathogens was measured using artificial inoculations in half-sib families of Norway spruce trees originating from central to northern Europe. The genetic component of resistance was analysed using 63,760 genome-wide exome-capture sequenced SNPs and multitrait genome-wide associations. No correlation was found for resistance to the two pathogens; however, associations were found between genomic variants and resistance traits with synergic or antagonist pleiotropic effects to both pathogens. Additionally, a latitudinal cline in resistance in the bark to H. annosum s.s. was found; trees from southern latitudes, with a later bud-set and thicker stem diameter, allowed longer lesions, but this was not the case for H. parviporum. In summary, this study detects genomic variants with pleiotropic effects which explain multiple disease resistance from a genic level and could be useful for selection of resistant trees to both pathogens. Furthermore, it highlights the need for additional research to understand the evolution of resistance traits to multiple pathogens in trees.

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.

The ace-1 Locus Is Amplified in All Resistant Anopheles gambiae Mosquitoes: Fitness Consequences of Homogeneous and Heterogeneous Duplications.

Gene copy-number variations are widespread in natural populations, but investigating their phenotypic consequences requires contemporary duplications under selection. Such duplications have been found at the ace-1 locus (encoding the organophosphate and carbamate insecticides' target) in the mosquito Anopheles gambiae (the major malaria vector); recent studies have revealed their intriguing complexity, consistent with the involvement of various numbers and types (susceptible or resistant to insecticide) of copies. We used an integrative approach, from genome to phenotype level, to investigate the influence of duplication architecture and gene-dosage on mosquito fitness. We found that both heterogeneous (i.e., one susceptible and one resistant ace-1 copy) and homogeneous (i.e., identical resistant copies) duplications segregated in field populations. The number of copies in homogeneous duplications was variable and positively correlated with acetylcholinesterase activity and resistance level. Determining the genomic structure of the duplicated region revealed that, in both types of duplication, ace-1 and 11 other genes formed tandem 203kb amplicons. We developed a diagnostic test for duplications, which showed that ace-1 was amplified in all 173 resistant mosquitoes analyzed (field-collected in several African countries), in heterogeneous or homogeneous duplications. Each type was associated with different fitness trade-offs: heterogeneous duplications conferred an intermediate phenotype (lower resistance and fitness costs), whereas homogeneous duplications tended to increase both resistance and fitness cost, in a complex manner. The type of duplication selected seemed thus to depend on the intensity and distribution of selection pressures. This versatility of trade-offs available through gene duplication highlights the importance of large mutation events in adaptation to environmental variation. This impressive adaptability could have a major impact on vector control in Africa.

The evolutionary fate of heterogeneous gene duplications: A precarious overdominant equilibrium between environment, sublethality and complementation.

Gene duplications occur at a high rate. Although most appear detrimental, some homogeneous duplications (identical gene copies) can be selected for beneficial increase in produced proteins. Heterogeneous duplications, which combine divergent alleles of a single locus, are seldom studied due to the paucity of empirical data. We investigated their role in an ongoing adaptive process at the ace-1 locus in Culex pipiens mosquitoes. We assessed the worldwide diversity of the ace-1 alleles (single-copy, susceptible S and insecticide-resistant R, and duplicated D that pair one S and one R copy), analysed their phylogeography and measured their fitness to understand their early dynamics using population genetics models. It provides a coherent and comprehensive evolutionary scenario. We show that D alleles are present in most resistant populations and display a higher diversity than R alleles (27 vs. 4). Most appear to result from independent unequal crossing-overs between local single-copy alleles, suggesting a recurrent process. Most duplicated alleles have a limited geographic distribution, probably resulting from their homozygous sublethality (HS phenotype). In addition, heterozygotes carrying different HS D alleles showed complementation, indicating different recessive lethal mutations. Due to mosaic insecticide control practices, balancing selection (overdominance) plays a key role in the early dynamics of heterogeneous duplicated alleles; it also favours a high local polymorphism of HS D alleles in natural populations (overdominance reinforced by complementation). Overall, our study shows that the evolutionary fate of heterogeneous duplications (and their long-term role) depends on finely balanced selective pressures due to the environment and to their genomic structure.

Relating fitness to long-term environmental variations in natura.

Quantifying links between ecological processes and adaptation dynamics in natura remains a crucial challenge. Many studies have documented the strength, form and direction of selection, and its variations in space and time, but only a few managed to link these variations to their proximal causes. This step is, however, crucial, if we are to understand how the variation in selective pressure affects adaptive allele dynamics in natural settings. We used data from a long-term survey (about 30 years) monitoring the adaptation to insecticides of Culex pipiens mosquitoes in Montpellier area (France), focusing on three resistance alleles of the Ester locus. We used a population genetics model taking temporal and spatial variations in selective pressure into account, to assess the quantitative relationships between variations in the proximal agent of selection (amounts of insecticide sprayed) and the fitness of resistance alleles. The response to variations in selective pressure was fast, and the alleles displayed different fitness-to-environment relationships: the analyses revealed that even slight changes in insecticide doses could induce changes in the strength and direction of selection, thus changing the fitness ranking of the adaptive alleles. They also revealed that selective pressures other than the insecticides used for mosquito control affected the resistance allele dynamics. These fitness-to-environment relationships, fast responses and continuous evolution limit our ability to predict the outcome of adaptive allele dynamics in a changing environment, but they clearly contribute to the maintenance of polymorphism in natural populations. Our study also emphasizes the necessity of long-term surveys in evolutionary ecology.

Population structure of Wolbachia and cytoplasmic introgression in a complex of mosquito species.

BACKGROUND: The maternally inherited bacterium Wolbachia often acts as a subtle parasite that manipulates insect reproduction, resulting potentially in reproductive isolation between host populations. Whilst distinct Wolbachia strains are documented in a group of evolutionarily closely related mosquitoes known as the Culex pipiens complex, their impact on mosquito population genetics remains unclear. To this aim, we developed a PCR-RFLP test that discriminates the five known Wolbachia groups found in this host complex. We further examined the Wolbachia genetic diversity, the variability in the coinherited host mitochondria and their partitioning among members of the Cx. pipiens complex, in order to assess the impact of Wolbachia on host population structure. RESULTS: There was a strong association between Wolbachia and mitochondrial haplotypes indicating a stable co-transmission in mosquito populations. Despite evidence that members of the Cx. pipiens complex are genetically distinct on the basis of nuclear DNA, the association of Wolbachia and mtDNA with members of the Cx. pipiens complex were limited. The Wolbachia wPip-I group, by far the most common, was associated with divergent Cx. pipiens members, including Cx. quinquefasciatus, Cx. pipiens pipiens form pipiens and Cx. pipiens pipiens form molestus. Four other wPip groups were also found in mosquito populations and all were shared between diverse Cx. pipiens members. CONCLUSION: This data overall supports the hypothesis that wPip infections, and their allied mitochondria, are associated with regular transfers between Cx. pipiens members rather than specific host associations. Overall, this is suggestive of a recent and likely ongoing cytoplasmic introgression through hybridization events across the Cx. pipiens complex.

A comprehensive framework for detecting copy number variants from single nucleotide polymorphism data: 'rCNV', a versatile r package for paralogue and CNV detection.

Recent studies have highlighted the significant role of copy number variants (CNVs) in phenotypic diversity, environmental adaptation and species divergence across eukaryotes. The presence of CNVs also has the potential to introduce genotyping biases, which can pose challenges to accurate population and quantitative genetic analyses. However, detecting CNVs in genomes, particularly in non-model organisms, presents a formidable challenge. To address this issue, we have developed a statistical framework and an accompanying r software package that leverage allelic-read depth from single nucleotide polymorphism (SNP) data for accurate CNV detection. Our framework capitalises on two key principles. First, it exploits the distribution of allelic-read depth ratios in heterozygotes for individual SNPs by comparing it against an expected distribution based on binomial sampling. Second, it identifies SNPs exhibiting an apparent excess of heterozygotes under Hardy-Weinberg equilibrium. By employing multiple statistical tests, our method not only enhances sensitivity to sampling effects but also effectively addresses reference biases, resulting in optimised SNP classification. Our framework is compatible with various NGS technologies (e.g. RADseq, Exome-capture). This versatility enables CNV calling from genomes of diverse complexities. To streamline the analysis process, we have implemented our framework in the user-friendly r package 'rCNV', which automates the entire workflow seamlessly. We trained our models using simulated data and validated their performance on four datasets derived from different sequencing technologies, including RADseq (Chinook salmon-Oncorhynchus tshawytscha), Rapture (American lobster-Homarus americanus), Exome-capture (Norway spruce-Picea abies) and WGS (Malaria mosquito-Anopheles gambiae).

Divergent selection predating the Last Glacial Maximum mainly acted on macro-phenotypes in Norway spruce.

The current distribution and population structure of many species were, to a large extent, shaped by cycles of isolation in glacial refugia and subsequent population expansions. Isolation in and postglacial expansion through heterogeneous environments led to either neutral or adaptive divergence. Norway spruce is no exception, and its current distribution is the consequence of a constant interplay between evolutionary and demographic processes. We investigated population differentiation and adaptation of Norway spruce for juvenile growth, diameter of the stem, wood density, and tracheid traits at breast height. Data from 4461 phenotyped and genotyped Norway spruce from 396 half-sib families in two progeny tests were used to test for divergent selection in the framework of Q ST vs. F ST. We show that the macroscopic resultant trait (stem diameter), unlike its microscopic components (tracheid dimensions) and juvenile growth, was under divergent selection that predated the Last Glacial Maximum. Altogether, the current variation in these phenotypic traits in Norway spruce is better explained by local adaptation to ancestral environments than to current ones, where populations were partly preadapted, mainly through growth-related traits.

BioRssay: an R package for analyses of bioassays and probit graphs.

Dose-response relationships reflect the effects of a substance on organisms, and are widely used in broad research areas, from medicine and physiology, to vector control and pest management in agronomy. Furthermore, reporting on the response of organisms to stressors is an essential component of many public policies (e.g. public health, environment), and assessment of xenobiotic responses is an integral part of World Health Organization recommendations. Building upon an R script that we previously made available, and considering its popularity, we have now developed a software package in the R environment, BioRssay, to efficiently analyze dose-response relationships. It has more user-friendly functions and more flexibility, and proposes an easy interpretation of the results. The functions in the BioRssay package are built on robust statistical analyses to compare the dose/exposure-response of various bioassays and effectively visualize them in probit-graphs.

Evolutionary trade-offs associated with copy number variations in resistance alleles in Culex pipiens mosquitoes.

Organophosphate and carbamate insecticides have largely been used worldwide to control mosquito populations. As a response, the same amino acid substitution in the ace-1 gene (G119S), conferring resistance to both insecticides, has been selected independently in many mosquito species. In Anopheles gambiae, it has recently been shown that the G119S mutation is actually part of homogeneous duplications that associate multiple resistance copies of the ace-1 gene. In this study, we showed that duplications of resistance copies of the ace-1 gene also exist in the Culex pipiens species complex. The number of copies is variable, and different numbers of copies are associated with different phenotypic trade-offs: we used a combination of bioassays and competition in population cages to show that having more resistance copies conferred higher resistance levels, but was also associated with higher selective disadvantage (or cost) in the absence of insecticide. These results further show the versatility of the genetic architecture of resistance to organophosphate and carbamate insecticides around the ace-1 locus and its role in fine-tuned adaptation to insecticide treatment variations.

Genomics and adaptation in forest ecosystems.

Rapid human-induced environmental changes like climate warming represent a challenge for forest ecosystems. Due to their biological complexity and the long generation time of their keystone tree species, genetic adaptation in these ecosystems might not be fast enough to keep track with conditions changing at such a fast pace. The study of adaptation to environmental change and its genetic mechanisms is therefore key for ensuring a sustainable support and management of forests. The 4-day conference of the European Research Group EvolTree (https://www.evoltree.eu) on the topic of "Genomics and Adaptation in Forest Ecosystems" brought together over 130 scientists to present and discuss the latest developments and findings in forest evolutionary research. Genomic studies in forest trees have long been hampered by the lack of high-quality genomics resources and affordable genotyping methods. This has dramatically changed in the last few years; the conference impressively showed how such tools are now being applied to study past demography, adaptation and interactions with associated organisms. Moreover, genomic studies are now finally also entering the world of conservation and forest management, for example by measuring the value or cost of interspecific hybridization and introgression, assessing the vulnerability of species and populations to future change, or accurately delineating evolutionary significant units. The newly launched conference series of EvolTree will hopefully play a key role in the exchange and synthesis of such important investigations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11295-022-01542-1.

The relative role of plasticity and demographic history in Capsella bursa-pastoris: a common garden experiment in Asia and Europe.

The colonization success of a species depends on the interplay between its phenotypic plasticity, adaptive potential and demographic history. Assessing their relative contributions during the different phases of a species range expansion is challenging, and requires large-scale experiments. Here, we investigated the relative contributions of plasticity, performance and demographic history to the worldwide expansion of the shepherd's purse, Capsella bursa-pastoris. We installed two large common gardens of the shepherd's purse, a young, self-fertilizing, allopolyploid weed with a worldwide distribution. One common garden was located in Europe, the other in Asia. We used accessions from three distinct genetic clusters (Middle East, Europe and Asia) that reflect the demographic history of the species. Several life-history traits were measured. To explain the phenotypic variation between and within genetic clusters, we analysed the effects of (i) the genetic clusters, (ii) the phenotypic plasticity and its association to fitness and (iii) the distance in terms of bioclimatic variables between the sampling site of an accession and the common garden, i.e. the environmental distance. Our experiment showed that (i) the performance of C. bursa-pastoris is closely related to its high phenotypic plasticity; (ii) within a common garden, genetic cluster was a main determinant of phenotypic differences; and (iii) at the scale of the experiment, the effect of environmental distance to the common garden could not be distinguished from that of genetic clusters. Phenotypic plasticity and demographic history both play important role at different stages of range expansion. The success of the worldwide expansion of C. bursa-pastoris was undoubtedly influenced by its strong phenotypic plasticity.