African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana

Over the past 20 y, many studies have examined the history of the plant ecological and molecular model, Arabidopsis thaliana, in Europe and North America. Although these studies informed us about the recent history of the species, the early history has remained elusive. In a large-scale genomic analysis of African A. thaliana, we sequenced the genomes of 78 modern and herbarium samples from Africa and analyzed these together with over 1,000 previously sequenced Eurasian samples. In striking contrast to expectations, we find that all African individuals sampled are native to this continent, including those from sub-Saharan Africa. Moreover, we show that Africa harbors the greatest variation and represents the deepest history in the A. thaliana lineage. Our results also reveal evidence that selfing, a major defining characteristic of the species, evolved in a single geographic region, best represented today within Africa. Demographic inference supports a model in which the ancestral A. thaliana population began to split by 120-90 kya, during the last interglacial and Abbassia pluvial, and Eurasian populations subsequently separated from one another at around 40 kya. This bears striking similarities to the patterns observed for diverse species, including humans, implying a key role for climatic events during interglacial and pluvial periods in shaping the histories and current distributions of a wide range of species

African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana

Over the past 20 y, many studies have examined the history of the plant ecological and molecular model, Arabidopsis thaliana, in Europe and North America. Although these studies informed us about the recent history of the species, the early history has remained elusive. In a large-scale genomic analysis of African A. thaliana, we sequenced the genomes of 78 modern and herbarium samples from Africa and analyzed these together with over 1,000 previously sequenced Eurasian samples. In striking contrast to expectations, we find that all African individuals sampled are native to this continent, including those from sub-Saharan Africa. Moreover, we show that Africa harbors the greatest variation and represents the deepest history in the A. thaliana lineage. Our results also reveal evidence that selfing, a major defining characteristic of the species, evolved in a single geographic region, best represented today within Africa. Demographic inference supports a model in which the ancestral A. thaliana population began to split by 120-90 kya, during the last interglacial and Abbassia pluvial, and Eurasian populations subsequently separated from one another at around 40 kya. This bears striking similarities to the patterns observed for diverse species, including humans, implying a key role for climatic events during interglacial and pluvial periods in shaping the histories and current distributions of a wide range of species.Peer Reviewe

Patterns of polymorphism and selection in the subgenomes of the allopolyploid Arabidopsis kamchatica

Genome duplication is widespread in wild and crop plants. However, little is known about genome-wide selection in polyploids due to the complexity of duplicated genomes. In polyploids, the patterns of purifying selection and adaptive substitutions may be affected by masking owing to duplicated genes or homeologs as well as effective population size. Here, we resequence 25 accessions of the allotetraploid Arabidopsis kamchatica, which is derived from the diploid species A. halleri and A. lyrata. We observe a reduction in purifying selection compared with the parental species. Interestingly, proportions of adaptive non-synonymous substitutions are significantly positive in contrast to most plant species. A recurrent pattern observed in both frequency and divergence–diversity neutrality tests is that the genome-wide distributions of both subgenomes are similar, but the correlation between homeologous pairs is low. This may increase the opportunity of different evolutionary trajectories such as in the HMA4 gene involved in heavy metal hyperaccumulation

Does Speciation between Arabidopsis halleri and Arabidopsis lyrata Coincide with Major Changes in a Molecular Target of Adaptation?

Ever since Darwin proposed natural selection as the driving force for the origin of species, the role of adaptive processes in speciation has remained controversial. In particular, a largely unsolved issue is whether key divergent ecological adaptations are associated with speciation events or evolve secondarily within sister species after the split. The plant Arabidopsis halleri is one of the few species able to colonize soils highly enriched in zinc and cadmium. Recent advances in the molecular genetics of adaptation show that the physiology of this derived ecological trait involves copy number expansions of the AhHMA4 gene, for which orthologs are found in single copy in the closely related A. lyrata and the outgroup A. thaliana. To gain insight into the speciation process, we ask whether adaptive molecular changes at this candidate gene were contemporary with important stages of the speciation process. We first inferred the scenario and timescale of speciation by comparing patterns of variation across the genomic backgrounds of A. halleri and A. lyrata. Then, we estimated the timing of the first duplication of AhHMA4 in A. halleri. Our analysis suggests that the historical split between the two species closely coincides with major changes in this molecular target of adaptation in the A. halleri lineage. These results clearly indicate that these changes evolved in A. halleri well before industrial activities fostered the spread of Zn- and Cd-polluted areas, and suggest that adaptive processes related to heavy-metal homeostasis played a major role in the speciation process

Contrasted Patterns of Molecular Evolution in Dominant and Recessive Self-Incompatibility Haplotypes in Arabidopsis

Self-incompatibility has been considered by geneticists a model system for reproductive biology and balancing selection, but our understanding of the genetic basis and evolution of this molecular lock-and-key system has remained limited by the extreme level of sequence divergence among haplotypes, resulting in a lack of appropriate genomic sequences. In this study, we report and analyze the full sequence of eleven distinct haplotypes of the self-incompatibility locus (S-locus) in two closely related Arabidopsis species, obtained from individual BAC libraries. We use this extensive dataset to highlight sharply contrasted patterns of molecular evolution of each of the two genes controlling self-incompatibility themselves, as well as of the genomic region surrounding them. We find strong collinearity of the flanking regions among haplotypes on each side of the S-locus together with high levels of sequence similarity. In contrast, the S-locus region itself shows spectacularly deep gene genealogies, high variability in size and gene organization, as well as complete absence of sequence similarity in intergenic sequences and striking accumulation of transposable elements. Of particular interest, we demonstrate that dominant and recessive S-haplotypes experience sharply contrasted patterns of molecular evolution. Indeed, dominant haplotypes exhibit larger size and a much higher density of transposable elements, being matched only by that in the centromere. Overall, these properties highlight that the S-locus presents many striking similarities with other regions involved in the determination of mating-types, such as sex chromosomes in animals or in plants, or the mating-type locus in fungi and green algae

Population genomics of transitions to selfing in brassicaceae model systems

Abstract Many plants harbor complex mechanisms that promote outcrossing and efficient pollen transfer. These include floral adaptations as well as genetic mechanisms, such as molecular self-incompatibility (SI) systems. The maintenance of such systems over long evolutionary timescales suggests that outcrossing is favorable over a broad range of conditions. Conversely, SI has repeatedly been lost, often in association with transitions to self-fertilization (selfing). This transition is favored when the short-term advantages of selfing outweigh the costs, primarily inbreeding depression. The transition to selfing is expected to have major effects on population genetic variation and adaptive potential, as well as on genome evolution. In the Brassicaceae, many studies on the population genetic, gene regulatory, and genomic effects of selfing have centered on the model plant Arabidopsis thaliana and the crucifer genus Capsella. The accumulation of population genomics datasets have allowed detailed investigation of where, when and how the transition to selfing occurred. Future studies will take advantage of the development of population genetics theory on the impact of selfing, especially regarding positive selection. Furthermore, investigation of systems including recent transitions to selfing, mixed mating populations and/or multiple independent replicates of the same transition will facilitate dissecting the effects of mating system variation from processes driven by demography