scholarly journals Inter-chromosomal linkage disequilibrium and linked fitness cost loci influence the evolution of nontarget site herbicide resistance in an agricultural weed

2021 ◽  
Author(s):  
Sonal Gupta ◽  
Alex Harkess ◽  
Anah Soble ◽  
Megan Van Etten ◽  
James Leebens-Mack ◽  
...  

The adaptation of weedy plants to herbicide is both a significant problem in agriculture and a model for the study of rapid adaptation under regimes of strong selection. Despite recent advances in our understanding of simple genetic changes that lead to resistance, a significant gap remains in our knowledge of resistance controlled by many loci and the evolutionary factors that influence the maintenance of resistance over time. Here, we perform a multi-level analysis involving whole genome sequencing and assembly, resequencing, and gene expression analysis to both uncover putative loci involved in nontarget herbicide resistance and to examine evolutionary forces underlying the maintenance of resistance in natural populations. We found loci involved in herbicide detoxification, stress sensing, and alterations in the shikimate acid pathway to be under selection, and confirmed that detoxification is responsible for glyphosate resistance using a functional assay. Furthermore, we found interchromosomal linkage disequilibrium (ILD), most likely associated with epistatic selection, to influence NTSR loci found on separate chromosomes thus potentially mediating resistance through generations. Additionally, by combining the selection screen, differential expression, and LD analysis, we identified fitness cost loci that are strongly linked to resistance alleles, indicating the role of genetic hitchhiking in maintaining the cost. Overall, our work strongly suggests that NTSR glyphosate resistance in I. purpurea is conferred by multiple genes which are maintained through generations via ILD and that the fitness cost associated with resistance in this species is a by-product of genetic-hitchhiking.

PLoS Genetics ◽  
2021 ◽  
Vol 17 (7) ◽  
pp. e1009676
Author(s):  
Jesse A. Garcia ◽  
Kirk E. Lohmueller

Evolutionary forces like Hill-Robertson interference and negative epistasis can lead to deleterious mutations being found on distinct haplotypes. However, the extent to which these forces depend on the selection and dominance coefficients of deleterious mutations and shape genome-wide patterns of linkage disequilibrium (LD) in natural populations with complex demographic histories has not been tested. In this study, we first used forward-in-time simulations to predict how negative selection impacts LD. Under models where deleterious mutations have additive effects on fitness, deleterious variants less than 10 kb apart tend to be carried on different haplotypes relative to pairs of synonymous SNPs. In contrast, for recessive mutations, there is no consistent ordering of how selection coefficients affect LD decay, due to the complex interplay of different evolutionary effects. We then examined empirical data of modern humans from the 1000 Genomes Project. LD between derived alleles at nonsynonymous SNPs is lower compared to pairs of derived synonymous variants, suggesting that nonsynonymous derived alleles tend to occur on different haplotypes more than synonymous variants. This result holds when controlling for potential confounding factors by matching SNPs for frequency in the sample (allele count), physical distance, magnitude of background selection, and genetic distance between pairs of variants. Lastly, we introduce a new statistic HR(j) which allows us to detect interference using unphased genotypes. Application of this approach to high-coverage human genome sequences confirms our finding that nonsynonymous derived alleles tend to be located on different haplotypes more often than are synonymous derived alleles. Our findings suggest that interference may play a pervasive role in shaping patterns of LD between deleterious variants in the human genome, and consequently influences genome-wide patterns of LD.


Plants ◽  
2019 ◽  
Vol 8 (11) ◽  
pp. 469 ◽  
Author(s):  
Vila-Aiub

Herbicide resistance is the ultimate evidence of the extraordinary capacity of weeds to evolve under stressful conditions. Despite the extraordinary plant fitness advantage endowed by herbicide resistance mutations in agroecosystems under herbicide selection, resistance mutations are predicted to exhibit an adaptation cost (i.e., fitness cost), relative to the susceptible wild-type, in herbicide untreated conditions. Fitness costs associated with herbicide resistance mutations are not universal and their expression depends on the particular mutation, genetic background, dominance of the fitness cost, and environmental conditions. The detrimental effects of herbicide resistance mutations on plant fitness may arise as a direct impact on fitness-related traits and/or coevolution with changes in other life history traits that ultimately may lead to fitness costs under particular ecological conditions. This brings the idea that a “lower adaptive value” of herbicide resistance mutations represents an opportunity for the design of resistance management practices that could minimize the evolution of herbicide resistance. It is evident that the challenge for weed management practices aiming to control, minimize, or even reverse the frequency of resistance mutations in the agricultural landscape is to “create” those agroecological conditions that could expose, exploit, and exacerbate those life history and/or fitness traits affecting the evolution of herbicide resistance mutations. Ideally, resistance management should implement a wide range of cultural practices leading to environmentally mediated fitness costs associated with herbicide resistance mutations.


Genetics ◽  
2000 ◽  
Vol 156 (1) ◽  
pp. 457-467 ◽  
Author(s):  
Z W Luo ◽  
S H Tao ◽  
Z-B Zeng

Abstract Three approaches are proposed in this study for detecting or estimating linkage disequilibrium between a polymorphic marker locus and a locus affecting quantitative genetic variation using the sample from random mating populations. It is shown that the disequilibrium over a wide range of circumstances may be detected with a power of 80% by using phenotypic records and marker genotypes of a few hundred individuals. Comparison of ANOVA and regression methods in this article to the transmission disequilibrium test (TDT) shows that, given the genetic variance explained by the trait locus, the power of TDT depends on the trait allele frequency, whereas the power of ANOVA and regression analyses is relatively independent from the allelic frequency. The TDT method is more powerful when the trait allele frequency is low, but much less powerful when it is high. The likelihood analysis provides reliable estimation of the model parameters when the QTL variance is at least 10% of the phenotypic variance and the sample size of a few hundred is used. Potential use of these estimates in mapping the trait locus is also discussed.


Genetics ◽  
2001 ◽  
Vol 157 (2) ◽  
pp. 899-909
Author(s):  
Rongling Wu ◽  
Zhao-Bang Zeng

Abstract A new strategy for studying the genome structure and organization of natural populations is proposed on the basis of a combined analysis of linkage and linkage disequilibrium using known polymorphic markers. This strategy exploits a random sample drawn from a panmictic natural population and the open-pollinated progeny of the sample. It is established on the principle of gene transmission from the parental to progeny generation during which the linkage between different markers is broken down due to meiotic recombination. The strategy has power to simultaneously capture the information about the linkage of the markers (as measured by recombination fraction) and the degree of their linkage disequilibrium created at a historic time. Simulation studies indicate that the statistical method implemented by the Fisher-scoring algorithm can provide accurate and precise estimates for the allele frequencies, recombination fractions, and linkage disequilibria between different markers. The strategy has great implications for constructing a dense linkage disequilibrium map that can facilitate the identification and positional cloning of the genes underlying both simple and complex traits.


1991 ◽  
Vol 48 (1) ◽  
pp. 60-66 ◽  
Author(s):  
Gary K. Meffe

Much light can be shed on life history evolution through study of responses of organisms to chronic exposure to a novel or perturbed environment. To determine the influence of 28 yr of temporally unpredictable thermal elevation on their life history patterns, I sampled eastern mosquitofish (Gambusia holbrooki) from a thermally elevated (outflow from a nuclear reactor) and an ambient (farm pond) habitat in South Carolina every month for 2 yr. Fish from the artificially heated environment reproduced all year, had higher reproductive investments (higher clutch sizes and reproductive biomass), and smaller offspring than did fish from the ambient environment, which ceased reproduction from October through March, typical for natural populations of the region. Likely environmental factors responsible for these differences include unpredictable food resources, higher mortality from thermal death, and higher predation by fishes and birds in the heated waters. The extent to which these life history alterations are the result of adaptive genetic changes versus phenotypically plastic responses remains to be tested.


2020 ◽  
Author(s):  
Benjamin J. Parker ◽  
Jan Hrček ◽  
Ailsa H.C. McLean ◽  
Jennifer A. Brisson ◽  
H. Charles J. Godfray

AbstractMany insects host vertically-transmitted microbes, which can confer benefits to their hosts but are costly to maintain and regulate. A key feature of these symbioses is variation: for example, symbiont density can vary among host and symbiont genotypes. However, the evolutionary forces maintaining this variation remain unclear. We studied variation in symbiont density using the pea aphid (Acyrthosiphon pisum) and the bacterium Regiella insecticola, a symbiont that can protect its host against fungal pathogens. We found that relative symbiont density varies both between two Regiella phylogenetic clades and among aphid ‘biotypes’. Higher-density symbiont infections are correlated with stronger survival costs, but variation in density has little effect on the protection Regiella provides against fungus. Instead, we found that in some aphid genotypes, a dramatic decline in symbiont density precedes the loss of a symbiont infection. Together, our data suggest that the optimal density of a symbiont infection is likely different from the perspective of aphid and microbial fitness. Regiella might prevent loss by maintaining high within-host densities, but hosts do not appear to benefit from higher symbiont numbers and may be advantaged by losing costly symbionts in certain environments. The standing variation in symbiont density observed in natural populations could therefore be maintained by antagonistic coevolutionary interactions between hosts and their symbiotic microbes.


2021 ◽  
Author(s):  
Daniel J. Cotter ◽  
Timothy H. Webster ◽  
Melissa A. Wilson

AbstractMutation, recombination, selection, and demography affect genetic variation across the genome. Increased mutation and recombination both lead to increases in genetic diversity in a region-specific manner, while complex demographic patterns shape patterns of diversity on a more global scale. The X chromosome is particularly interesting because it contains several distinct regions that are subject to different combinations and strengths of these processes, notably the pseudoautosomal regions (PARs) and the X-transposed region (XTR). The X chromosome thus can serve as a unique model for studying how genetic and demographic forces act in different contexts to shape patterns of observed variation. Here we investigate diversity, divergence, and linkage disequilibrium in each region of the X chromosome using genomic data from 26 human populations. We find that both diversity and substitution rate are consistently elevated in PAR1 and the XTR compared to the rest of the X chromosome. In contrast, linkage disequilibrium is lowest in PAR1 and highest on the non-recombining X chromosome, with the XTR falling in between, suggesting that the XTR (usually included in the non-recombining X) may need to be considered separately in future studies. We also observed strong population-specific effects on genetic diversity; not only does genetic variation differ on the X and autosomes among populations, but the effects of linked selection on the X relative to autosomes have been shaped by population-specific history. The substantial variation in patterns of variation across these regions provides insight into the unique evolutionary history contained within the X chromosome.Significance StatementDemography and selection affect the X chromosome differently from non-sex chromosomes. However, the X chromosome can be subdivided into multiple distinct regions that facilitate even more fine-scaled assessment of these processes. Here we study regions of the human X chromosome in 26 populations to find evidence that recombination may be mutagenic in humans and that the X-transposed region may undergo recombination. Further we observe that the effects of selection and demography act differently on the X chromosome relative to the autosomes across human populations. Together, our results highlight profound regional differences across the X chromosome, simultaneously making it an ideal system for exploring the action of evolutionary forces as well as necessitating its careful consideration and treatment in genomic analyses.


Author(s):  
Daniel L. Hartl

This chapter could as well be titled “Population Genomics,” although many aspects of population genomics are integrated throughout the other chapters. It includes estimates of mutational variance and standing variance, phenotypic evolution under directional selection as measured by the linear selection gradient, and phenotypic evolution under stabilizing selection. It explores the strengths and limitations of genome-wide association studies of quantitative trait loci (QTLs) and expression (eQTLs) to detect genetic influencing complex traits in natural populations and genetic risk factors for complex diseases such as heart disease or diabetes. The number of genes affecting complex traits is considered, as well as evidence bearing on the issue of whether complex diseases are primarily affected by a very large number of genes, almost all of small effect, and how this bears on direct-to-consumer and over-the-counter genetic testing. The population genomics of adaptation is considered, including drug resistance, domestication, and local selection versus gene flow. The chapter concludes with the population genomics of speciation as illustrated by reinforcement of mating barriers, the reproducibility of phenotypic and genetic changes, and the accumulation of genetic incompatibilities.


2020 ◽  
Vol 10 (5) ◽  
pp. 1553-1561 ◽  
Author(s):  
Garrett McKinney ◽  
Megan V. McPhee ◽  
Carita Pascal ◽  
James E. Seeb ◽  
Lisa W. Seeb

Many studies exclude loci that exhibit linkage disequilibrium (LD); however, high LD can signal reduced recombination around genomic features such as chromosome inversions or sex-determining regions. Chromosome inversions and sex-determining regions are often involved in adaptation, allowing for the inheritance of co-adapted gene complexes and for the resolution of sexually antagonistic selection through sex-specific partitioning of genetic variants. Genomic features such as these can escape detection when loci with LD are removed; in addition, failing to account for these features can introduce bias to analyses. We examined patterns of LD using network analysis to identify an overlapping chromosome inversion and sex-determining region in chum salmon. The signal of the inversion was strong enough to show up as false population substructure when the entire dataset was analyzed, while the effect of the sex-determining region on population structure was only obvious after restricting analysis to the sex chromosome. Understanding the extent and geographic distribution of inversions is now a critically important part of genetic analyses of natural populations. Our results highlight the importance of analyzing and understanding patterns of LD in genomic dataset and the perils of excluding or ignoring loci exhibiting LD. Blindly excluding loci in LD would have prevented detection of the sex-determining region and chromosome inversion while failing to understand the genomic features leading to high-LD could have resulted in false interpretations of population structure.


2019 ◽  
Vol 3 (Supplement_1) ◽  
pp. S234-S234
Author(s):  
Daniel Promislow

Abstract Advances in whole genome sequencing have dramatically increased our potential to understand what shapes variation in rates of aging and age-related disease in natural populations, but we are still far from realizing this potential. Researchers have identified thousands of genetic markers associated with complex human traits. However, these markers typically explain a very small fraction of the observed variance, leaving an enormous explanatory gap between genotype and phenotype. I will present data from diverse species to illustrate the power of so-called endophenotypes—the epigenome, transcriptome, proteome, and metabolome—to bridge the genotype-phenotype gap. Using multivariate and network models that integrate genetic information with other endophenotype variation, we are closer than ever to understanding the mechanisms that account for natural variation in aging and age-related disease, and the evolutionary forces that have shaped that variation.


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