The transition from outcrossing to self-fertilization is one of the most common evolutionary changes in plants, yet only about 10–15% of flowering plants are predominantly selfing. To explain this ...phenomenon, Stebbins proposed that selfing may be an ‘evolutionary dead end’. According to this hypothesis, transitions from outcrossing to selfing are irreversible, and selfing lineages suffer from an increased risk of extinction owing to a reduced potential for adaptation. Thus, although selfing can be advantageous in the short term, selfing lineages may be mostly short-lived owing to higher extinction rates. Here, we review recent results relevant to the ‘dead-end hypothesis’ of selfing and the maintenance of outcrossing over longer evolutionary time periods. In particular, we highlight recent results regarding diversification rates in self-incompatible and self-compatible taxa, and review evidence regarding the accumulation of deleterious mutations in selfing lineages. We conclude that while some aspects of the hypothesis of selfing as a dead end are supported by theory and empirical results, the evolutionary and ecological mechanisms remain unclear. We highlight the need for more studies on the effects of quantitative changes in outcrossing rates and on the potential for adaptation, particularly in selfing plants. In addition, there is growing evidence that transitions to selfing may themselves be drivers of speciation, and future studies of diversification and speciation should investigate this further.
Coevolution between transposable elements and recombination Kent, Tyler V.; Uzunović, Jasmina; Wright, Stephen I.
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
12/2017, Letnik:
372, Številka:
1736
Journal Article
Recenzirano
Odprti dostop
One of the most striking patterns of genome structure is the tight, typically negative, association between transposable elements (TEs) and meiotic recombination rates. While this is a highly ...recurring feature of eukaryotic genomes, the mechanisms driving correlations between TEs and recombination remain poorly understood, and distinguishing cause versus effect is challenging. Here, we review the evidence for a relation between TEs and recombination, and discuss the underlying evolutionary forces. Evidence to date suggests that overall TE densities correlate negatively with recombination, but the strength of this correlation varies across element types, and the pattern can be reversed. Results suggest that heterogeneity in the strength of selection against ectopic recombination and gene disruption can drive TE accumulation in regions of low recombination, but there is also strong evidence that the regulation of TEs can influence local recombination rates. We hypothesize that TE insertion polymorphism may be important in driving within-species variation in recombination rates in surrounding genomic regions. Furthermore, the interaction between TEs and recombination may create positive feedback, whereby TE accumulation in non-recombining regions contributes to the spread of recombination suppression. Further investigation of the coevolution between recombination and TEs has important implications for our understanding of the evolution of recombination rates and genome structure.
This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.
Evolutionary theory predicts that factors such as a small population size or low recombination rate can limit the action of natural selection. The emerging field of comparative population genomics ...offers an opportunity to evaluate these hypotheses. However, classical theoretical predictions assume that populations are at demographic equilibrium. This assumption is likely to be violated in the very populations researchers use to evaluate selection's limits: populations that have experienced a recent shift in population size and/or effective recombination rates. Here we highlight theory and data analyses concerning limitations on the action of natural selection in nonequilibrial populations and argue that substantial care is needed to appropriately test whether species and populations show meaningful differences in selection efficacy. A move toward model-based inferences that explicitly incorporate nonequilibrium dynamics provides a promising approach to more accurately contrast selection efficacy across populations and interpret its significance.
The evolution of herbicide resistance in weed populations is a highly replicated example of adaptation surmounting the race against extinction, but the factors determining its rate and nature remain ...poorly understood. Here, we explore theory and empirical evidence for the importance of population genetic parameters-including effective population size, dominance, mutational target size, and gene flow-in influencing the probability and mode of herbicide resistance adaptation and its variation across species. We compiled data on the number of resistance mutations across populations for 79 herbicide-resistant species. Our findings are consistent with theoretical predictions that self-fertilization reduces resistance adaptation from standing variation within populations, but increases independent adaptation across populations. Furthermore, we provide evidence for a ploidy-mating system interaction that may reflect trade-offs in polyploids between increased effective population size and greater masking of beneficial mutations. We highlight the power of population genomic approaches to provide insights into the evolutionary dynamics of herbicide resistance with important implications for understanding the limits of adaptation.
Abstract
Accurate estimates of genome-wide rates and fitness effects of new mutations are essential for an improved understanding of molecular evolutionary processes. Although eukaryotic genomes ...generally contain a large noncoding fraction, functional noncoding regions and fitness effects of mutations in such regions are still incompletely characterized. A promising approach to characterize functional noncoding regions relies on identifying accessible chromatin regions (ACRs) tightly associated with regulatory DNA. Here, we applied this approach to identify and estimate selection on ACRs in Capsella grandiflora, a crucifer species ideal for population genomic quantification of selection due to its favorable population demography. We describe a population-wide ACR distribution based on ATAC-seq data for leaf samples of 16 individuals from a natural population. We use population genomic methods to estimate fitness effects and proportions of positively selected fixations (α) in ACRs and find that intergenic ACRs harbor a considerable fraction of weakly deleterious new mutations, as well as a significantly higher proportion of strongly deleterious mutations than comparable inaccessible intergenic regions. ACRs are enriched for expression quantitative trait loci (eQTL) and depleted of transposable element insertions, as expected if intergenic ACRs are under selection because they harbor regulatory regions. By integrating empirical identification of intergenic ACRs with analyses of eQTL and population genomic analyses of selection, we demonstrate that intergenic regulatory regions are an important source of nearly neutral mutations. These results improve our understanding of selection on noncoding regions and the role of nearly neutral mutations for evolutionary processes in outcrossing Brassicaceae species.
Understanding the evolutionary forces that shape genetic variation within species has long been a goal of evolutionary biology. Integrating data for the genetic architecture of traits from ...genome-wide association mapping studies (GWAS) along with the development of new population genetic methods for identifying selection in sequence data may allow us to evaluate the roles of mutation–selection balance and balancing selection in shaping genetic variation at various scales. Here,wereview the theoretical predictions for genetic architecture and additional signals of selection on genomic sequence for the loci that affect traits. Next,we reviewhow plant GWAS have tested for the signatures of various selective scenarios. Limited evidence to date suggests that within-population variation is maintained primarily by mutation–selection balance while variation across the landscape is the result of local adaptation. However, there are a number of inherent biases in these interpretations. We highlight these challenges and suggest ways forward to further understanding of the maintenance of variation.
The shift from outcrossing to self-fertilization is among the most common evolutionary transitions in flowering plants. Until recently, however, a genome-wide view of this transition has been ...obscured by both a dearth of appropriate data and the lack of appropriate population genomic methods to interpret such data. Here, we present a novel population genomic analysis detailing the origin of the selfing species, Capsella rubella, which recently split from its outcrossing sister, Capsella grandiflora. Due to the recency of the split, much of the variation within C. rubella is also found within C. grandiflora. We can therefore identify genomic regions where two C. rubella individuals have inherited the same or different segments of ancestral diversity (i.e. founding haplotypes) present in C. rubella's founder(s). Based on this analysis, we show that C. rubella was founded by multiple individuals drawn from a diverse ancestral population closely related to extant C. grandiflora, that drift and selection have rapidly homogenized most of this ancestral variation since C. rubella's founding, and that little novel variation has accumulated within this time. Despite the extensive loss of ancestral variation, the approximately 25% of the genome for which two C. rubella individuals have inherited different founding haplotypes makes up roughly 90% of the genetic variation between them. To extend these findings, we develop a coalescent model that utilizes the inferred frequency of founding haplotypes and variation within founding haplotypes to estimate that C. rubella was founded by a potentially large number of individuals between 50 and 100 kya, and has subsequently experienced a twenty-fold reduction in its effective population size. As population genomic data from an increasing number of outcrossing/selfing pairs are generated, analyses like the one developed here will facilitate a fine-scaled view of the evolutionary and demographic impact of the transition to self-fertilization.
• Clonal propagation allows some plant species to achieve massive population sizes quickly but also reduces the evolutionary independence of different sites in the genome.
• We examine genome-wide ...genetic diversity in Spirodela polyrhiza, a duckweed that reproduces primarily asexually.
• We find that this geographically widespread and numerically abundant species has very low levels of genetic diversity. Diversity at nonsynonymous sites relative to synonymous sites is high, suggesting that purifying selection is weak. A potential explanation for this observation is that a very low frequency of sex renders selection ineffective. However, there is a pronounced decay in linkage disequilibrium over 40 kb, suggesting that though sex may be rare at the individual level it is not too infrequent at the population level. In addition, neutral diversity is affected by the physical proximity of selected sites, which would be unexpected if sex was exceedingly rare at the population level.
• The amount of genetic mixing as assessed by the decay in linkage disequilibrium is not dissimilar from selfing species such as Arabidopsis thaliana, yet selection appears to be much less effective in duckweed. We discuss alternative explanations for the signature of weak purifying selection.
Elucidating the genetic basis of morphological changes in evolution remains a major challenge in biology 1–3. Repeated independent trait changes are of particular interest because they can indicate ...adaptation in different lineages or genetic and developmental constraints on generating morphological variation 4–6. In animals, changes to “hot spot” genes with minimal pleiotropy and large phenotypic effects underlie many cases of repeated morphological transitions 4–8. By contrast, only few such genes have been identified from plants 8–11, limiting cross-kingdom comparisons of the principles of morphological evolution. Here, we demonstrate that the REDUCED COMPLEXITY (RCO) locus 12 underlies more than one naturally evolved change in leaf shape in the Brassicaceae. We show that the difference in leaf margin dissection between the sister species Capsella rubella and Capsella grandiflora is caused by cis-regulatory variation in the homeobox gene RCO-A, which alters its activity in the developing lobes of the leaf. Population genetic analyses in the ancestral C. grandiflora indicate that the more-active C. rubella haplotype is derived from a now rare or lost C. grandiflora haplotype via additional mutations. In Arabidopsis thaliana, the deletion of the RCO-A and RCO-B genes has contributed to its evolutionarily derived smooth leaf margin 12, suggesting the RCO locus as a candidate for an evolutionary hot spot. We also find that temperature-responsive expression of RCO-A can explain the phenotypic plasticity of leaf shape to ambient temperature in Capsella, suggesting a molecular basis for the well-known negative correlation between temperature and leaf margin dissection.
•Leaf shape evolution in Capsella is due to altered expression of a homeobox gene•The high-lobing allele likely arose by novel mutation in Capsella rubella•RCO-A mediates phenotypic plasticity of leaf shape to ambient temperature
Leaf shape varies greatly among plant species and is modulated by the environment. Sicard et al. demonstrate that altered expression of a homeobox gene underlies different leaf shapes between two species of shepherd’s purse (Capsella). The temperature-responsive expression of this gene mediates plasticity of leaf shape to ambient temperature.
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.
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