Population genomic and historical analysis suggests a global invasion by bridgehead processes in Mimulus guttatus.
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ABSTRACT:
SUBMITTER: Vallejo-Marin M
PROVIDER: S-EPMC7954805 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Across western North America, Mimulus guttatus exists as many local populations adapted to site-specific environmental challenges. Gene flow between locally adapted populations will affect genetic diversity both within demes and across the larger metapopulation. Here, we analyse 34 whole-genome sequences from the intensively studied Iron Mountain population (IM) in conjunction with sequences from 22 Mimulus individuals sampled from across western North America. Three striking features of these data address hypotheses about migration and selection in a locally adapted population. First, we find very high levels of intrapopulation polymorphism (synonymous π = 0.033). Variation outside of genes is likely even higher but difficult to estimate because excessive divergence reduces the efficiency of read mapping. Second, IM exhibits a significantly positive genomewide average for Tajima's D. This indicates allele frequencies are typically more intermediate than expected from neutrality, opposite the pattern observed in many other species. Third, IM exhibits a distinctive haplotype structure with a genomewide excess of positive associations between rarer alleles at linked loci. This suggests an important effect of gene flow from other Mimulus populations, although a residual effect of population founding might also contribute. The combination of multiple analyses, including a novel tree-based analytic method, illustrates how the balance of local selection, limited dispersal and metapopulation dynamics manifests across the genome. The overall genomic pattern of sequence diversity suggests successful gene flow of divergent immigrant genotypes into IM. However, many loci show patterns indicative of local adaptation, particularly at SNPs associated with chromosomal inversions.
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Project description:The molecular signature of selection depends strongly on whether new mutations are immediately favorable and sweep to fixation (hard sweeps) as opposed to when selection acts on segregating variation (soft sweeps). The prediction of reduced sequence variation around selected polymorphisms is much stronger for hard than soft sweeps, particularly when considering quantitative traits where sweeps are likely to be incomplete. Here, we directly investigate the genomic signal of soft sweeps within an artificial selection experiment on Mimulus guttatus. We first develop a statistical method based on Fisher's angular transformation of allele frequencies to identify selected loci. Application of this method identifies about 400 significant windows, but no fixed differences between phenotypically divergent populations. With two notable exceptions, we find a modest average effect of partial sweeps on the amount of molecular variation. The first exception is a polymorphic inversion on chromosome 6. The increase of the derived haplotype has a broad genomic effect due to recombination suppression coupled with substantial initial haplotype structure within the population. Second, we found significant increases in nucleotide variation around selected loci in the population evolving larger flowers. This suggests that "high" alleles for flower size were initially less frequent than "low" alleles. This result is consistent with prior studies of M. guttatus and illustrates how molecular evolution can depend on the allele frequency spectrum at quantitative trait loci.
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Project description:Major unresolved questions in evolutionary genetics include determining the contributions of different mutational sources to the total pool of genetic variation in a species, and understanding how these different forms of genetic variation interact with natural selection. Recent work has shown that structural variants (SVs) (insertions, deletions, inversions, and transpositions) are a major source of genetic variation, often outnumbering single nucleotide variants in terms of total bases affected. Despite the near ubiquity of SVs, major questions about their interaction with natural selection remain. For example, how does the allele frequency spectrum of SVs differ when compared with single nucleotide variants? How often do SVs affect genes, and what are the consequences? To begin to address these questions, we have systematically identified and characterized a large set of submicroscopic insertion and deletion (indel) variants (between 1 and 200 kb in length) among ten inbred lines from a single natural population of the plant species Mimulus guttatus. After extensive computational filtering, we focused on a set of 4,142 high-confidence indels that showed an experimental validation rate of 73%. All but one of these indels were less than 200 kb. Although the largest were generally at lower frequencies in the population, a surprising number of large indels are at intermediate frequencies. Although indels overlapping with genes were much rarer than expected by chance, approximately 600 genes were affected by an indel. Nucleotide-binding site leucine-rich repeat (NBS-LRR) defense response genes were the most enriched among the gene families affected. Most indels associated with genes were rare and appeared to be under purifying selection, though we do find four high-frequency derived insertion alleles that show signatures of recent positive selection.
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Project description:Mimulus guttatus and M. nasutus are an evolutionary and ecological model sister species pair differentiated by ecology, mating system, and partial reproductive isolation. Despite extensive research on this system, the history of divergence and differentiation in this sister pair is unclear. We present and analyze a population genomic data set which shows that M. nasutus budded from a central Californian M. guttatus population within the last 200 to 500 thousand years. In this time, the M. nasutus genome has accrued genomic signatures of the transition to predominant selfing, including an elevated proportion of nonsynonymous variants, an accumulation of premature stop codons, and extended levels of linkage disequilibrium. Despite clear biological differentiation, we document genomic signatures of ongoing, bidirectional introgression. We observe a negative relationship between the recombination rate and divergence between M. nasutus and sympatric M. guttatus samples, suggesting that selection acts against M. nasutus ancestry in M. guttatus.
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Project description:The degree to which genomic architecture varies across space and time is central to the evolution of genomes in response to natural selection. Bulked-segregant mapping combined with pooled sequencing provides an efficient means to estimate the effect of genetic variants on quantitative traits. We develop a novel likelihood framework to identify segregating variation within multiple populations and generations while accommodating estimation error on a sample- and SNP-specific basis. We use this method to map loci for flowering time within natural populations of Mimulus guttatus, collecting the early- and late-flowering plants from each of three neighboring populations and two consecutive generations. Structural variants, such as inversions, and genes from multiple flowering-time pathways exhibit the strongest associations with flowering time. We find appreciable variation in genetic effects on flowering time across both time and space; the greatest differences evident between populations, where numerous factors (environmental variation, genomic background, and private polymorphisms) likely contribute to heterogeneity. However, the changes across years within populations clearly identify genotype-by-environment interactions as an important influence on flowering time variation.
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Project description:Anthropogenic perturbations including habitat loss and emerging disease are changing pollinator communities and generating novel selection pressures on plant populations. Disruption of plant-pollinator relationships is predicted to cause plant mating system evolution, although this process has not been directly observed. This study demonstrates the immediate evolutionary effects of pollinator loss within experimental populations of a predominately outcrossing wildflower. Initially equivalent populations evolved for five generations within two pollination treatments: abundant bumblebee pollinators versus no pollinators. The populations without pollinators suffered greatly reduced fitness in early generations but rebounded as they evolved an improved ability to self-fertilize. All populations diverged in floral, developmental, and life-history traits, but only a subset of characters showed clear association with pollination treatment. Pronounced treatment effects were noted for anther-stigma separation and autogamous seed set. Dramatic allele frequency changes at two chromosomal polymorphisms occurred in the no pollinator populations, explaining a large fraction of divergence in pollen viability. The pattern of phenotypic and genetic changes in this experiment favors a sequential model for the evolution of the multitrait "selfing syndrome" observed throughout angiosperms.
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Project description:Inbreeding in plants typically reduces individual fitness but may also alter ecological interactions. This study examined the effect of inbreeding in the mixed-mating annual Mimulus guttatus on visitation by pollinators (Bombus impatiens) in greenhouse experiments. Previous studies of M. guttatus have shown that inbreeding reduced corolla size, flower number, and pollen quantity and quality. Using controlled crosses, we produced inbred and outbred families from three different M. guttatus populations. We recorded the plant genotypes that bees visited and the number of flowers probed per visit. In our first experiment, bees were 31% more likely to visit outbred plants than those selfed for one generation and 43% more likely to visit outbred plants than those selfed for two generations. Inbreeding had only a small effect on the number of flowers probed once bees arrived at a genotype. These differences were explained partially by differences in mean floral display and mean flower size, but even when these variables were controlled statistically, the effect of inbreeding remained large and significant. In a second experiment we quantified pollen viability from inbred and self plants. Bees were 37-54% more likely to visit outbred plants, depending on the population, even when controlling for floral display size. Pollen viability proved to be as important as floral display in predicting pollinator visitation in one population, but the overall explanatory power of a multiple regression model was weak. Our data suggested that bees use cues in addition to display size, flower size, and pollen reward quality in their discrimination of inbred plants. Discrimination against inbred plants could have effects on plant fitness and thereby reinforce selection for outcrossing. Inbreeding in plant populations could also reduce resource quality for pollinators, potentially resulting in negative effects on pollinator populations.
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Project description:Small RNAs (21-24 nt) are pivotal regulators of gene expression that guide both transcriptional and post-transcriptional silencing mechanisms in diverse eukaryotes, including most if not all plants. MicroRNAs (miRNAs) and short interfering RNAs (siRNAs) are the two major types, both of which have a demonstrated and important role in plant development, stress responses and pathogen resistance. In this work, we used a deep sequencing approach (Sequencing-By-Synthesis, or SBS) to develop sequence resources of small RNAs from Mimulus guttatus tissues (including leaves, flowers and roots). The high depth of the resulting datasets enabled us to examine in detail critical small RNA features as size distribution, tissue-specific regulation and sequence conservation between different organs in this species. We also developed database resources and a dedicated website (http://smallrna.udel.edu/) with computational tools for allowing other users to identify new miRNAs or siRNAs involved in specific regulatory pathways, verify the degree of conservation of these sequences in other plant species and map small RNAs on genes or larger regions of the maize genome under study.
2011-05-10 | GSE28971 | GEO
Project description:Chromosomal rearrangement polymorphisms are common and increasingly found to be associated with adaptive ecological divergence and speciation. Rearrangements, such as inversions, reduce recombination in heterozygous individuals and thus can protect favourable allelic combinations at linked loci, facilitating their spread in the presence of gene flow. Recently, we identified a chromosomal inversion polymorphism that contributes to ecological adaptation and reproductive isolation between annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus. Here we evaluate the population genetic structure of this inverted region in comparison with the collinear regions of the genome across the M. guttatus species complex. We tested whether annual and perennial M. guttatus exhibit different patterns of divergence for loci in the inverted and noninverted regions of the genome. We then evaluated whether there are contrasting climate associations with these genomic regions through redundancy analysis. We found that the inversion exhibits broadly different patterns of divergence among annual and perennial M. guttatus and is associated with environmental variation across population accessions. This study is the first widespread population genetic survey of the diversity of the M. guttatus species complex. Our findings contribute to a greater understanding of morphological, ecological, and genetic evolutionary divergence across this highly diverse group of closely related ecotypes and species. Finally, understanding species relationships among M. guttatus sp. has hitherto been stymied by accumulated evidence of substantial gene flow among populations as well as designated species. Nevertheless, our results shed light on these relationships and provide insight into adaptation in life history traits within the complex.
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Project description:Evolution of genetic (co)variances (the G-matrix) fundamentally influences multitrait divergence. Here, we isolated the contribution of two chromosomal quantitative trait loci (QTLs), a meiotic drive locus and a polymorphic inversion, to the overall G-matrix for a suite of floral, phenological and male fitness traits in a population of Mimulus guttatus. This allowed us to predict the evolution of trait means and genetic (co)variances as a function of allele frequencies, and to evaluate theories about the maintenance of genetic variation in fitness. Individuals generated using a replicated F(2) breeding design were grown under common conditions, genotyped and measured for trait values. Significant additive genetic variance existed for all traits, and most genetic covariances were significantly nonzero. Both QTLs contribute to the additive genetic (co)variances of multiple traits. Pleiotropy was not generally consistent, either between QTLs or with the genetic background. Shifts in allele frequencies at either QTL are predicted to result in substantial changes in the G-matrix. Both QTLs contribute substantially to the genetic variation in pollen viability. The Drive QTL, and perhaps also the inversion, demonstrates the contribution of balancing selection to the maintenance of genetic variation in fitness.
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