Ploidy-variable species allow direct inference of the effects of chromosome copy number on fundamental evolutionary processes. While an abundance of theoretical work suggests polyploidy should leave distinct population genomic signatures, empirical data remains sparse. We sequenced ~300 individuals from 39 populations of Arabidopsis arenosa, a naturally diploid-autotetraploid species. We find the impacts of polyploidy on population genomic processes are subtle yet pervasive, including reduced efficiency on linked and purifying selection as well as rampant gene flow from diploids. Initial masking of deleterious mutations, faster rates of nucleotide substitution, and interploidy introgression all conspire to shape the evolutionary potential of polyploids.
Genes for which homologs can be detected only in a limited group of evolutionarily related species, called “lineage-specific genes,” are pervasive: Essentially every lineage has them, and they often comprise a sizable fraction of the group’s total genes. Lineage-specific genes are often interpreted as “novel” genes, representing genetic novelty born anew within that lineage. Here, we develop a simple method to test an alternative null hypothesis: that lineage-specific genes do have homologs outside of the lineage that, even while evolving at a constant rate in a novelty-free manner, have merely become undetectable by search algorithms used to infer homology. We show that this null hypothesis is sufficient to explain the lack of detected homologs of a large number of lineage-specific genes in fungi and insects. However, we also find that a minority of lineage-specific genes in both clades are not well explained by this novelty-free model. The method provides a simple way of identifying which lineage-specific genes call for special explanations beyond homology detection failure, highlighting them as interesting candidates for further study.
Serpentine barrens represent extreme hazards for plant colonists. These sites are characterized by high porosity leading to drought, lack of essential mineral nutrients, and phytotoxic levels of metals. Nevertheless, nature forged populations adapted to these challenges. Here, we use a population-based evolutionary genomic approach coupled with elemental profiling to assess how autotetraploid Arabidopsis arenosa adapted to a multichallenge serpentine habitat in the Austrian Alps. We first demonstrate that serpentine-adapted plants exhibit dramatically altered elemental accumulation levels in common conditions, and then resequence 24 autotetraploid individuals from three populations to perform a genome scan. We find evidence for highly localized selective sweeps that point to a polygenic, multitrait basis for serpentine adaptation. Comparing our results to a previous study of independent serpentine colonizations in the closely related diploid Arabidopsis lyrata in the United Kingdom and United States, we find the highest levels of differentiation in 11 of the same loci, providing candidate alleles for mediating convergent evolution. This overlap between independent colonizations in different species suggests that a limited number of evolutionary strategies are suited to overcome the multiple challenges of serpentine adaptation. Interestingly, we detect footprints of selection in A. arenosa in the context of substantial gene flow from nearby off-serpentine populations of A. arenosa, as well as from A. lyrata. In several cases, quantitative tests of introgression indicate that some alleles exhibiting strong selective sweep signatures appear to have been introgressed from A. lyrata. This finding suggests that migrant alleles may have facilitated adaptation of A. arenosa to this multihazard environment.adaptation | plant | gene flow | population genomics S erpentine barrens offer powerful venues for the study of multitrait adaptations. Soils at these sites feature dramatically skewed elemental contents, phytotoxic levels of heavy metals, drought risk, and very poor mineral nutrition (1-3). A defining characteristic of serpentine soils is a greatly reduced Ca:Mg ratio along with low K, N, and P, resulting in severe ion homeostasis challenges for plant colonists (4-6). Serpentine soils are also highly porous and thus chronically drought prone. As a result of these challenges, serpentine barrens are characterized by minimal ecosystem productivity and high rates of endemism (reviewed in refs. 2 and 3). Evolution has nevertheless repeatedly forged plant populations that overcome these hazards, making serpentine sites an important natural model for ecology, evolution, and physiology. Given the quantifiable challenges of serpentine adaptation presented by strongly skewed elemental levels and dehydration risk, adapted populations present a valuable opportunity to identify loci underlying adaptations important for understanding basic evolutionary processes, as well as candidate genes for rational crop design for tolerance of ...
Weediness in ephemeral plants is commonly characterized by rapid cycling, prolific all-in flowering, and loss of perenniality. Many species made transitions to weediness of this sort, which can be advantageous in high-disturbance or human-associated habitats. The molecular basis of this shift, however, remains mostly mysterious. Here, we use transcriptome sequencing, genome resequencing scans for selection, and stress tolerance assays to study a weedy population of the otherwise nonweedy Arabidopsis arenosa, an obligately outbreeding relative of Arabidopsis thaliana. Although weedy A. arenosa is widespread, a single genetic lineage colonized railways throughout central and northern Europe. We show that railway plants, in contrast to plants from sheltered outcrops in hill/mountain regions, are rapid cycling, have lost the vernalization requirement, show prolific flowering, and do not return to vegetative growth. Comparing transcriptomes of railway and mountain plants across time courses with and without vernalization, we found that railway plants have sharply abrogated vernalization responsiveness and high constitutive expression of heat-and cold-responsive genes. Railway plants also have strong constitutive heat shock and freezing tolerance compared with mountain plants, where tolerance must be induced. We found 20 genes with good evidence of selection in the railway population. One of these, LATE ELONGATED HYPOCOTYL, is known in A. thaliana to regulate many stress-response genes that we found to be differentially regulated among the distinct habitats. Our data suggest that, beyond life history regulation, other traits like basal stress tolerance also are associated with the evolution of weediness in A. arenosa.Life history traits differ between and within plant species and commonly reflect the requirements of the habitats in which they are found (Baker, 1974;Weinig et al., 2003;Grime, 2006). Depending on abiotic and biotic conditions, a variety of strategies can be favored, and accordingly, weeds are phenotypically diverse. In environments that are unpredictable, with frequent occurrences of stresses like drought, temperature fluctuations, or human-associated perturbations, rapid cycling and early flowering are common (Hall and Willis, 2006;Sherrard and Maherali, 2006;Franks et al., 2007;Wu et al., 2010). Life history adaptations can help mediate tradeoffs between resource accumulation and stress avoidance and are important for wild species as well as for crops (Jung and Müller, 2009). Comparing results among species, as well as the correlates of these traits with other fitness-related traits, promises new insights into the mechanisms of adaptation to unpredictable habitats.A common phenotype of plants in unpredictable habitats is early and prolific flowering relative to related populations in more stable habitats (Baker, 1965; Grotkopp et al
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