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The Arctic is one of the most extreme terrestrial environments on the planet. Here, we present the first chromosome‐scale genome assembly of a plant adapted to the high Arctic, Draba nivalis (Brassicaceae), an attractive model species for studying plant adaptation to the stresses imposed by this harsh environment. We used an iterative scaffolding strategy with data from short‐reads, single‐molecule long reads, proximity ligation data, and a genetic map to produce a 302 Mb assembly that is highly contiguous with 91.6% assembled into eight chromosomes (the base chromosome number). To identify candidate genes and gene families that may have facilitated adaptation to Arctic environmental stresses, we performed comparative genomic analyses with nine non‐Arctic Brassicaceae species. We show that the D. nivalis genome contains expanded suites of genes associated with drought and cold stress (e.g., related to the maintenance of oxidation‐reduction homeostasis, meiosis, and signaling pathways). The expansions of gene families associated with these functions appear to be driven in part by the activity of transposable elements. Tests of positive selection identify suites of candidate genes associated with meiosis and photoperiodism, as well as cold, drought, and oxidative stress responses. Our results reveal a multifaceted landscape of stress adaptation in the D. nivalis genome, offering avenues for the continued development of this species as an Arctic model plant., see also the Perspective by Tanja Pyhäjärvi and Tiina M. Mattila

Supergenes govern balanced polymorphisms in a wide range of systems. The reciprocal placement of stigmas and anthers in pin and thrum floral morphs of distylous species constitutes an iconic example of a balanced polymorphism governed by a supergene, the distyly S-locus. Recent studies have shown that the Primula and Turnera distyly supergenes are both hemizygous in thrums, but it remains unknown if hemizygosity is pervasive among distyly S-loci. Here we have characterized the genetic architecture and evolution of the distyly supergene in Linum by generating a chromosome-level genome assembly of Linum tenue, followed by the identification of the S-locus using population genomic data. We show that hemizygosity and thrum-specific expression of S-linked genes, including a pistil-expressed candidate gene for style length, are major features of the Linum S-locus. Structural variation is likely instrumental for recombination suppression, and although the non-recombining dominant haplotype has accumulated transposable elements, S-linked genes are not under relaxed purifying selection. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes. The chromosome-level genome assembly and detailed characterization of the distyly S-locus in L. tenue will facilitate elucidation of molecular mechanisms underlying the different forms of flowers described by Darwin.

Fertilization in angiosperms involves the germination of pollen on the stigma, followed by the extrusion of a pollen tube that elongates through the style and delivers two sperm cells to the embryo sac. Sexual selection could occur throughout this process when male gametophytes compete for fertilization. The strength of sexual selection during pollen competition should be affected by the number of genotypes deposited on the stigma. As increased self-fertilization reduces the number of mating partners, and the genetic diversity and heterozygosity of populations, it should thereby reduce the intensity of sexual selection during pollen competition. Despite the prevalence of mating system shifts, few studies have directly compared the molecular signatures of sexual selection during pollen competition in populations with different mating systems. Here we analyzed whole-genome sequences from natural populations of Arabis alpina, a species showing mating system variation across its distribution, to test whether shifts from cross- to self-fertilization result in molecular signatures consistent with sexual selection on genes involved in pollen competition. We found evidence for efficient purifying selection on genes expressed in vegetative pollen, and overall weaker selection on sperm-expressed genes. This pattern was robust when controlling for gene expression level and specificity. In agreement with the expectation that sexual selection intensifies under cross-fertilization, we found that the efficacy of purifying selection on male gametophyte-expressed genes was significantly stronger in genetically more diverse and outbred populations. Our results show that intra-sexual competition shapes the evolution of pollen-expressed genes, and that its strength fades with increasing self-fertilization rates.

Parallel adaptation provides valuable insight into the predictability of evolutionary change through replicated natural experiments. A steadily increasing number of studies have demonstrated genomic parallelism, yet the magnitude of this parallelism varies depending on whether populations, species, or genera are compared. This led us to hypothesize that the magnitude of genomic parallelism scales with genetic divergence between lineages, but whether this is the case and the underlying evolutionary processes remain unknown. Here, we resequenced seven parallel lineages of two Arabidopsis species, which repeatedly adapted to challenging alpine environments. By combining genome-wide divergence scans with model-based approaches, we detected a suite of 151 genes that show parallel signatures of positive selection associated with alpine colonization, involved in response to cold, high radiation, short season, herbivores, and pathogens. We complemented these parallel candidates with published gene lists from five additional alpine Brassicaceae and tested our hypothesis on a broad scale spanning ∼0.02 to 18 My of divergence. Indeed, we found quantitatively variable genomic parallelism whose extent significantly decreased with increasing divergence between the compared lineages. We further modeled parallel evolution over the Arabidopsis candidate genes and showed that a decreasing probability of repeated selection on the same standing or introgressed alleles drives the observed pattern of divergence-dependent parallelism. We therefore conclude that genetic divergence between populations, species, and genera, affecting the pool of shared variants, is an important factor in the predictability of genome evolution.

Demography determines the strength of genetic drift, which generally reduces genetic variation and the efficacy of selection. Here, we disentangled the importance of demographic processes at a local scale (census size and mating system) and at a species-range scale (old split between population clusters, recolonization after the last glaciation cycle, and admixture) in determining within-population genomic diversity and genomic signatures of positive selection. Analyses were based on re-sequence data from 52 populations of North American Arabidopsis lyrata collected across its entire distribution. The mating system and range dynamics since the last glaciation cycle explained around 60% of the variation in genomic diversity among populations and 52% of the variation in the signature of positive selection. Diversity was lowest in selfing compared with outcrossing populations and in areas further away from glacial refugia. In parallel, reduced positive selection was found in selfing populations and in populations with a longer route of postglacial range expansion. The signature of positive selection was also reduced in populations without admixture. We conclude that recent range expansion can have a profound influence on diversity in coding and non-coding DNA, similar in magnitude to the shift toward selfing. Distribution limits may in fact be caused by reduced effective population size and compromised positive selection in recently colonized parts of the range., Demography is predicted to affect the magnitude of genetic drift, which in turn lowers the efficacy of directional selection. Across the geographic distribution of a plant, this study shows that the mating system and past species range dynamics, in particular postglacial range expansion, explain population-level genetic variation and the genome-wide signature of positive selection. Selfing populations and those with longer expansion routes have greatly reduced the signatures of selection, pointing to evolutionary constraints in adaptation.

Polyploidy, or whole-genome duplication, is a common speciation mechanism in plants. An important barrier to polyploid establishment is a lack of compatible mates. Because self-compatibility alleviates this problem, it has long been hypothesized that there should be an association between polyploidy and self-compatibility (SC), but empirical support for this prediction is mixed. Here, we investigate whether the molecular makeup of the Brassicaceae self-incompatibility (SI) system, and specifically dominance relationships among S-haplotypes mediated by small RNAs, could facilitate loss of SI in allopolyploid crucifers. We focus on the allotetraploid species Capsella bursa-pastoris, which formed ~300 kya by hybridization and whole-genome duplication involving progenitors from the lineages of Capsella orientalis and Capsella grandiflora. We conduct targeted long-read sequencing to assemble and analyze eight full-length S-locus haplotypes, representing both homeologous subgenomes of C. bursa-pastoris. We further analyze small RNA (sRNA) sequencing data from flower buds to identify candidate dominance modifiers. We find that C. orientalis-derived S-haplotypes of C. bursa-pastoris harbor truncated versions of the male SI specificity gene SCR and express a conserved sRNA-based candidate dominance modifier with a target in the C. grandiflora-derived S-haplotype. These results suggest that pollen-level dominance may have facilitated loss of SI in C. bursa-pastoris. Finally, we demonstrate that spontaneous somatic tetraploidization after a wide cross between C. orientalis and C. grandiflora can result in production of self-compatible tetraploid offspring. We discuss the implications of this finding on the mode of formation of this widespread weed.

Parallel adaptation provides valuable insight into the predictability of evolutionary change through replicated natural experiments. A steadily increasing number of studies have demonstrated genomic parallelism, yet the magnitude of this parallelism varies depending on whether populations, species or genera are compared. This led us to hypothesize that the magnitude of genomic parallelism scales with genetic divergence between lineages, but whether this is the case and the underlying evolutionary processes remain unknown. Here, we resequenced seven parallel lineages of twoArabidopsisspecies which repeatedly adapted to challenging alpine environments. By combining genome-wide divergence scans with model-based approaches we detected a suite of 151 genes that show parallel signatures of positive selection associated with alpine colonization, involved in response to cold, high radiation, short season, herbivores and pathogens. We complemented these parallel candidates with published gene lists from five additional alpine Brassicaceae and tested our hypothesis on a broad scale spanning ~ 0.02 to 18 million years of divergence. Indeed, we found quantitatively variable genomic parallelism whose extent significantly decreased with increasing divergence between the compared lineages. We further modeled parallel evolution over theArabidopsiscandidate genes and showed that a decreasing probability of repeated selection of the same standing or introgressed alleles drives the observed pattern of divergence-dependent parallelism. We therefore conclude that genetic divergence between populations, species and genera, affecting the pool of shared variants, is an important factor in the predictability of genome evolution.Significance statementRepeated evolution tends to be more predictable. The impressive spectrum of recent reports on genomic parallelism, however, revealed that the fraction of the genome that evolves in parallel largely varies, possibly reflecting different evolutionary scales investigated. Here, we demonstrate divergence-dependent parallelism using a comprehensive genome-wide dataset comprising 12 cases of parallel alpine adaptation and identify decreasing probability of adaptive re-use of genetic variation as the major underlying cause. This finding empirically demonstrates that evolutionary predictability is scale dependent and suggests that availability of pre-existing variation drives parallelism within and among populations and species. Altogether, our results inform the ongoing discussion about the (un)predictability of evolution, relevant for applications in pest control, nature conservation, or the evolution of pathogen resistance.

Understanding the factors that govern the distribution of species is a central goal of evolutionary ecology. It is commonly assumed that geographic range limits reflect ecological niche limits and that species experience increasingly marginal conditions towards the edge of their ranges. Using spatial data and ecological niche models we tested these hypotheses in Arabidopsis lyrata. Specifically, we asked whether range limits coincide with predicted niche limits in this system and whether the suitability of sites declines towards the edge of the species’ range in North America. We further explored patterns of environmental change towards the edge of the range and asked whether genome-wide patterns of genetic diversity decline with increasing peripherality and environmental marginality. Our results suggest that latitudinal range limits coincide with niche limits. Populations experienced increasingly marginal environments towards these limits – though patterns of environmental change were more complex than most theoretical models for range limits assume. Genomic diversity declined towards the edge of the species’ range and with increasing distance from the estimated centre of the species’ niche in environmental space, but not with the suitability of sites based on niche model predictions. Thus while latitudinal range limits in this system are broadly associated with niche limits, the link between environmental conditions and genetic diversity (and thus the adaptive potential of populations) is less clear.

Why species have geographically restricted distributions is an unresolved question in ecology and evolutionary biology. Here, we test a new explanation that mutation accumulation due to small population size or a history of range expansion can contribute to restricting distributions by reducing population growth rate at the edge. We examined genomic diversity and mutational load across the entire geographic range of the North American plant Arabidopsis lyrata, including old, isolated populations predominantly at the southern edge and regions of postglacial range expansion at the northern and southern edges. Genomic diversity in intergenic regions declined toward distribution edges and signatures of mutational load in exon regions increased. Genomic signatures of mutational load were highly linked to phenotypically expressed load, measured as reduced performance of individual plants and lower estimated rate of population growth. The geographic pattern of load and the connection between load and population growth demonstrate that mutation accumulation reduces fitness at the edge and helps restrict species’ distributions. distribution limits, genetic drift, genetic load, geographic expansion, leading edge, mutation accumulation, range limits, trailing edge

Shifts from outcrossing to self-fertilisation have occurred repeatedly in many different lineages of flowering plants, and often involve the breakdown of genetic outcrossing mechanisms. In the Brassicaceae, self-incompatibility (SI) allows plants to ensure outcrossing by recognition and rejection of self-pollen on the stigma. This occurs through the interaction of female and male specificity components, consisting of a pistil based receptor and a pollen-coat protein, both of which are encoded by tightly linked genes at theS-locus. When benefits of selfing are higher than costs of inbreeding, theory predicts that loss-of-function mutations in the male (pollen) SI component should be favoured, especially if they are dominant. However, it remains unclear whether mutations in the male component of SI are predominantly responsible for shifts to self-compatibility, and testing this prediction has been difficult due to the challenges of sequencing the highly polymorphic and repetitive ~100 kbpS-locus. The crucifer genusCapsellaoffers an excellent opportunity to study multiple transitions from outcrossing to self-fertilization, but so far, little is known about the genetic basis and timing of loss of SI in the self-fertilizing diploidCapsella orientalis. Here, we show that loss of SI inC. orientalisoccurred within the past 2.6 Mya and maps as a dominant trait to theS-locus. Using targeted long-read sequencing of multiple complete S-haplotypes, we identify a frameshift deletion in the male specificity geneSCRthat is fixed inC. orientalis, and we confirm loss of male SI specificity. We further analyze RNA sequencing data to identify a conserved,S-linked small RNA (sRNA) that is predicted to cause dominance of self-compatibility. Our results suggest that degeneration of pollen SI specificity in dominantS-alleles is important for shifts to self-fertilization in the Brassicaceae.Author SummaryAlready Darwin was fascinated by the widely varying modes of plant reproduction. The shift from outcrossing to self-fertilization is considered one of the most frequent evolutionary transitions in flowering plants, yet we still know little about the genetic basis of these shifts. In the Brassicaceae, outcrossing is enforced by a self-incompatibility (SI) system that enables the recognition and rejection of self pollen. This occurs through the action of two tightly linked genes at theS-locus, that encode a receptor protein located on the stigma (female component) and a pollen ligand protein (male component), respectively. Nevertheless, SI has frequently been lost, and theory predicts that mutations in the male component should have an advantage during the loss of SI, especially if they are dominant. To test this hypothesis, we mapped the loss of SI in a selfing species from the genusCapsella, a model system for evolutionary genomics. We found that loss of SI mapped to theS-locus, which harbored a dominant loss-of-function mutation in the male SI protein, and as expected, we found that male specificity was indeed lost inC. orientalis. Our results suggest that transitions to selfing often involve parallel genetic changes.

The CPB2 gene encodes thrombin-activatable fibrinolysis inhibitor (TAFI), a hepatically secreted zymogen acting as a molecular link among coagulation, fibrinolysis, and inflammation. Variants in CPB2 have been associated with several human conditions. We resequenced and analyzed the two regions carrying previously known nonsynonimous single-nucleotide polymorphisms (Ala147Thr and Ile325Thr) and variants affecting transcript stability. Our data indicate that whereas the gene portion extending from exon 9 to the 3' untranslated region fits a model of neutral evolution, variants in the region encompassing exons 6-7 have been maintained by balancing selection. Indeed, we verified that the region displays high nucleotide diversity, many intermediate frequency variants, and an excess of polymorphism compared with interspecific divergence. Consistently, haplotype analysis indicated the presence of two major haplotype clades separated by deep branches. Transcript analysis revealed that in both HepG2 cells and human liver samples, CPB2 exon 7 undergoes haplotype-preferential skipping. Therefore, we indicate that balancing selection has been maintaining functional variants that promote alternative exon 7 splicing. Although transcripts lacking exon 7 represent a minority of total CPB2 products, the effect on antifibrinolytic activity might be much greater as the intrinsic instability of TAFI is a major determinant of its antifibrinolytic potential. These data highlight the contribution of population genetics approaches to the analysis of functional genetic variation and may orient further biochemical and genetics studies on the pathophysiologic role of CPB2 gene products.

Molecules involved in leukocyte trafficking have a central role in the development of inflammatory and immune responses. We performed F(ST) analysis of the selectin cluster, as well as of SELPLG, ICAM1 and VCAM1. Peaks of significantly high population genetic differentiation were restricted to two regions in SELP and one in SELPLG. Resequencing data indicated that the region covering SELP exons 11-13 displays high nucleotide diversity in Africans and Europeans (CEU), and a high level of within-species diversity compared with inter-specific divergence. Analysis of inferred haplotypes revealed a complex phylogeny with two deeply separated clades that coalesce at ~3.5 million years (MY) plus a minor clade with a TMRCA (time to the most recent common ancestor) of ~2.2 MY. A splicing assay indicated no haplotype-specific effect on SELP exon 14 inclusion. These data are consistent with a model of multiallelic balancing selection; single-nucleotide polymorphism analysis indicated that the Val640Leu variant represents a likely selection target. In populations of Asian ancestry a distinct haplotype, possibly carrying regulatory variants, has been driven to high frequency by positive selection. No deviation from neutrality was observed for the SELPLG region. Resequencing of SELP in chimpanzees revealed a haplotype phylogeny with extremely deep basal branches, suggesting either long-standing balancing selection or ancestral population structure. Thus, SELP has experienced a complex selective history, possibly as a result of local adaptation. Variants in the gene have been associated with autoimmune and cardiovascular diseases. Association studies would benefit from both taking the complex SELP haplotype structure into account and from analysis of possible regulatory variants in the gene.

Although, plant breeding has been extremely successful at improving the yield of maize, quality has received less attention. However, important advances were made by breeders in this area as well, resulting in maize with a wide range of compositions. In fact, by exploiting genetic variation, the composition of the kernel was altered for both the quantity and quality (structure and chemical diversity) of starch, protein, and oil throughout kernel development. Furthermore, the ability of plant scientists to use existing genetic variation and to identify and manipulate commercially important genes will open new avenues to design novel variation in grain composition. This will provide the basis for the development of the next generation of speciality in maize and of new products to meet future needs.

Supergenes govern multi-trait-balanced polymorphisms in a wide range of systems; however, our understanding of their origins and evolution remains incomplete. The reciprocal placement of stigmas and anthers in pin and thrum floral morphs of distylous species constitutes an iconic example of a balanced polymorphism governed by a supergene, the distyly S-locus. Recent studies have shown that the Primula and Turnera distyly supergenes are both hemizygous in thrums, but it remains unknown whether hemizygosity is pervasive among distyly S-loci. As hemizygosity has major consequences for supergene evolution and loss, clarifying whether this genetic architecture is shared among distylous species is critical. Here, we have characterized the genetic architecture and evolution of the distyly supergene in Linum by generating a chromosome-level genome assembly of Linum tenue, followed by the identification of the S-locus using population genomic data. We show that hemizygosity and thrum-specific expression of S-linked genes, including a pistil-expressed candidate gene for style length, are major features of the Linum S-locus. Structural variation is likely instrumental for recombination suppression, and although the non-recombining dominant haplotype has accumulated transposable elements, S-linked genes are not under relaxed purifying selection. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes, provide a counterexample to classic inversion-based supergenes, and shed new light on the origin and maintenance of an iconic floral polymorphism., European Research Council (ERC) 757451 Swedish Research Council European Commission, Bergstroms foundation Carl Tryggers grant Knut and Alice Wallenberg Foundation as part of the National Bioinformatics Infrastructure Sweden at SciLifeLab, National Genomics Infrastructure (NGI) in Stockholm and Uppsala (Uppsala Genome Center, SNP&SEQ) - Knut and Alice Wallenberg Foundation, Science for Life Laboratory, Swedish Research Council, European Commission 2018-05973, NBIS (National Bioinformatics Infrastructure Sweden)