scholarly journals Repeated origins, gene flow, and allelic interactions of herbicide resistance mutations in a widespread agricultural weed

2021 ◽  
Author(s):  
Julia M Kreiner ◽  
George Sandler ◽  
Aaron J Stern ◽  
Patrick J. Tranel ◽  
Detlef Weigel ◽  
...  
Keyword(s):  
Gene Flow ◽  
Herbicide Resistance ◽  
De Novo ◽  
Parallel Evolution ◽  
Selective Advantage ◽  
Past Century ◽  
Resistance Mutations ◽  
Standing Variation ◽  
Agricultural Weed

Causal mutations and their frequency in nature are well-characterized for herbicide resistance. However, we still lack understanding of the extent of parallelism in the mutational origin of target-site resistance (TSR), the role of standing variation and gene flow in the spread of TSR variants, and allelic interactions that mediate their selective advantage. We addressed these questions with genomic data from 18 agricultural populations of Amaranthus tuberculatus, which we show to have undergone a massive expansion over the past century, with a contemporary Ne estimate of 8x107. We found nine TSR variants, three of which were common—showing extreme parallelism in mutational origin and an important role of gene flow in their geographic spread. The number of repeated origins varied across TSR loci and generally showed stronger signals of selection on de novo mutations, but with considerable evidence for selection on standing variation. Allele ages at TSR loci varied from ~10-250 years old, greatly predating the advent of herbicides. The evolutionary history of TSR has also been shaped by both intra- and inter-locus allelic interactions. We found evidence of haplotype competition between two TSR mutations, their successes in part modulated by either adaptive introgression of, or epistasis with, genome-wide resistance alleles. Together, this work reveals a remarkable example of spatial parallel evolution—the ability of independent mutations to spread due to selection contingent on not only the time, place, and background on which they arise but the haplotypes they encounter.

scholarly journals Extreme parallel evolution of flagellar motility is facilitated by synonymous sequence

2021 ◽  
Author(s):  
James S. Horton ◽  
Robert W. Jackson ◽  
Nicholas K. Priest ◽  
Tiffany B. Taylor
Keyword(s):  
De Novo ◽  
Parallel Evolution ◽  
Selective Advantage ◽  
Antagonistic Pleiotropy ◽  
Flagellar Motility ◽  
Kinase Gene ◽  
Evolutionary Rescue ◽  
Nucleotide Resolution ◽  
Competition Assays

AbstractIn recent years increasing interest has been shown in ‘forecasting’ evolution. Parallel evolution studies are crucial towards realising this goal because they are, by their very nature, easy to forecast. However, the causal role of identified drivers of parallel evolution – competitive selective advantage, mutational accessibility or heterogeneity in de novo mutation – remain unresolved. Here we show that synonymous sequences facilitates extreme parallel evolution during the evolutionary rescue of flagellar motility. An immotile variant of the soil microbe, Pseudomonas fluorescens, swiftly recovers flagellum-dependent motility through parallel de novo mutation. This typically manifests within 96 h under strong selection through repeatable mutation within the nitrogen pathway’s histidine kinase gene, ntrB. We found that mutation was often parallel to nucleotide resolution, with lineages fixing the same mutation (ntrB A289C) in over 95% of cases in minimal medium (M9). This repeatable de novo mutation was robust to nutrient condition despite evidence for antagonistic pleiotropy across nutrient regimes. Competition assays against alternative motile alleles revealed some evidence for selection enforcing repeated fixation of ntrB mutants, but there was no evidence for clonal interference driving parallel evolution to nucleotide resolution. Instead, we discovered evidence for extremely localised heterogeneity in de novo mutation. The introduction of 6 synonymous substitutions surrounding the mutational hotspot reduced parallel evolution from >95% to 0% at the site. Our results reveal that unique quirks in how DNA is structured at specific loci can strongly bias evolutionary outcomes and ensure extreme repeatability.

scholarly journals Standing genetic variation fuels rapid evolution of herbicide resistance in blackgrass

2021 ◽  
Author(s):  
Sonja Kersten ◽  
Jiyang Chang ◽  
Christian D Huber ◽  
Yoav Voichek ◽  
Christa Lanz ◽  
...  
Keyword(s):  
Genetic Variation ◽  
Herbicide Resistance ◽  
Large Scale ◽  
De Novo ◽  
Bulked Segregant Analysis ◽  
Target Site ◽  
Temperate Climate ◽  
Minor Role ◽  
Standing Variation ◽  
Target Site Resistance

Repeated herbicide applications exert enormous selection on blackgrass (Alopecurus myosuroides), a major weed in cereal crops of the temperate climate zone including Europe. This inadvertent large-scale experiment gives us the opportunity to look into the underlying genetic mechanisms and evolutionary processes of rapid adaptation, which can occur both through mutations in the direct targets of herbicides and through changes in other, often metabolic, pathways, known as non-target-site resistance. How much either type of adaptation relies on de novo mutations versus pre-existing standing variation is important for developing strategies to manage herbicide resistance. We generated a chromosome-level reference genome for A. myosuroides for population genomic studies of herbicide resistance and genome-wide diversity across Europe in this species. Bulked-segregant analysis evidenced that non-target-site resistance has a complex genetic architecture. Through empirical data and simulations, we showed that, despite its simple genetics, target-site resistance mainly results from standing genetic variation, with only a minor role for de novo mutations.

scholarly journals A Few Stickleback Suffice for the Transport of Alleles to New Lakes

2019 ◽  
Vol 10 (2) ◽  
pp. 505-514 ◽  
Author(s):  
Jared Galloway ◽  
William A. Cresko ◽  
Peter Ralph
Keyword(s):  
Gene Flow ◽  
Local Adaptation ◽  
De Novo ◽  
Empirical Studies ◽  
Low Frequency ◽  
Small Fish ◽  
Marine Population ◽  
Standing Variation ◽  
Population Genomic ◽  
Genomic Studies

Threespine stickleback populations provide a striking example of local adaptation to divergent habitats in populations that are connected by recurrent gene flow. These small fish occur in marine and freshwater habitats throughout the Northern Hemisphere, and in numerous cases the smaller freshwater populations have been established “de novo” from marine colonists. Independently evolved freshwater populations exhibit similar phenotypes that have been shown to derive largely from the same standing genetic variants. Geographic isolation prevents direct migration between the freshwater populations, strongly suggesting that these shared locally adaptive alleles are transported through the marine population. However it is still largely unknown how gene flow, recombination, and selection jointly impact the standing variation that might fuel this adaptation. Here we use individual-based, spatially explicit simulations to determine the levels of gene flow that best match observed patterns of allele sharing among habitats in stickleback. We aim to better understand how gene flow and local adaptation in large metapopulations determine the speed of adaptation and re-use of standing genetic variation. In our simulations we find that repeated adaptation uses a shared set of alleles that are maintained at low frequency by migration-selection balance in oceanic populations. This process occurs over a realistic range of intermediate levels of gene flow that match previous empirical population genomic studies in stickleback. Examining these simulations more deeply reveals how lower levels of gene flow leads to slow, independent adaptation to different habitats, whereas higher levels of gene flow leads to significant mutation load – but an increased probability of successful population genomic scans for locally adapted alleles. Surprisingly, we find that the genealogical origins of most freshwater adapted alleles can be traced back to the original generation of marine individuals that colonized the lakes, as opposed to subsequent migrants. These simulations provide deeper context for existing studies of stickleback evolutionary genomics, and guidance for future empirical studies in this model. More broadly, our results support existing theory of local adaptation but extend it by more completely documenting the genealogical history of adaptive alleles in a metapopulation.

scholarly journals Rapid parallel adaptation despite gene flow in silent crickets

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Xiao Zhang ◽  
Jack G. Rayner ◽  
Mark Blaxter ◽  
Nathan W. Bailey
Keyword(s):  
Gene Expression ◽  
Gene Flow ◽  
Expression Analysis ◽  
Gene Expression Analysis ◽  
De Novo ◽  
Parallel Evolution ◽  
De Novo Mutation ◽  
Genome Scans ◽  
Wing Structures ◽  
In The Wild

AbstractGene flow is predicted to impede parallel adaptation via de novo mutation, because it can introduce pre-existing adaptive alleles from population to population. We test this using Hawaiian crickets (Teleogryllus oceanicus) in which ‘flatwing’ males that lack sound-producing wing structures recently arose and spread under selection from an acoustically-orienting parasitoid. Morphometric and genetic comparisons identify distinct flatwing phenotypes in populations on three islands, localized to different loci. Nevertheless, we detect strong, recent and ongoing gene flow among the populations. Using genome scans and gene expression analysis we find that parallel evolution of flatwing on different islands is associated with shared genomic hotspots of adaptation that contain the gene doublesex, but the form of selection differs among islands and corresponds to known flatwing demographics in the wild. We thus show how parallel adaptation can occur on contemporary timescales despite gene flow, indicating that it could be less constrained than previously appreciated.

scholarly journals Gene expression shapes the patterns of parallel evolution of herbicide resistance in the agricultural weed Monochoria vaginalis

2021 ◽  
Author(s):  
Shinji Tanigaki ◽  
Akira Uchino ◽  
Shigenori Okawa ◽  
Chikako Miura ◽  
Kenshiro Hamamura ◽  
...  
Keyword(s):  
Gene Expression ◽  
Herbicide Resistance ◽  
Parallel Evolution ◽  
Agricultural Weed

scholarly journals Rapid Parallel Evolution of Azole Fungicide Resistance in Australian Populations of the Wheat Pathogen Zymoseptoria tritici

2018 ◽  
Vol 85 (4) ◽  
Author(s):  
Megan C. McDonald ◽  
Melanie Renkin ◽  
Merrin Spackman ◽  
Beverley Orchard ◽  
Daniel Croll ◽  
...  
Keyword(s):  
Gene Flow ◽  
Fungicide Resistance ◽  
De Novo ◽  
Parallel Evolution ◽  
Large Body ◽  
Septoria Tritici Blotch ◽  
Septoria Tritici ◽  
Whole Genome ◽  
Zymoseptoria Tritici ◽  
Content Type

ABSTRACT Zymoseptoria tritici is a globally distributed fungal pathogen which causes Septoria tritici blotch on wheat. Management of the disease is attempted through the deployment of resistant wheat cultivars and the application of fungicides. However, fungicide resistance is commonly observed in Z. tritici populations, and continuous monitoring is required to detect breakdowns in fungicide efficacy. We recently reported azole-resistant isolates in Australia; however, it remained unknown whether resistance was brought into the continent through gene flow or whether resistance emerged independently. To address this question, we screened 43 isolates across five Australian locations for azole sensitivity and performed whole-genome sequencing on 58 isolates from seven locations to determine the genetic basis of resistance. Population genomic analyses showed extremely strong differentiation between the Australian population recovered after azoles began to be used and both Australian populations recovered before azoles began to be used and populations on different continents. The apparent absence of recent gene flow between Australia and other continents suggests that azole fungicide resistance has evolved de novo and subsequently spread within Tasmania. Despite the isolates being distinct at the whole-genome level, we observed combinations of nonsynonymous substitutions at the CYP51 locus identical to those observed elsewhere in the world. We observed nine previously reported nonsynonymous mutations as well as isolates that carried a combination of the previously reported L50S, S188N, A379G, I381V, Y459DEL, G460DEL, and N513K substitutions. Assays for the 50% effective concentration against a subset of isolates exposed to the tebuconazole and epoxiconazole fungicides showed high levels of azole resistance. The rapid, parallel evolution of a complex CYP51 haplotype that matches a dominant European haplotype demonstrates the enormous potential for de novo resistance emergence in pathogenic fungi. IMPORTANCE Fungicides are essential to control diseases in agriculture because many crops are highly susceptible to pathogens. However, many pathogens rapidly evolve resistance to fungicides. A large body of studies have described specific mutations conferring resistance and have often made inferences about the origins of resistance based on sequencing data from the target gene alone. Here, we show the de novo acquisition of resistance to the ubiquitously used azole fungicides in genetically isolated populations of the wheat pathogen Zymoseptoria tritici in Tasmania, Australia. We confirm evidence for parallel evolution through genome-scale analyses of representative worldwide populations. The emergence of complex resistance haplotypes following a well-documented recent introduction of azoles into Australian farming practices demonstrates how rapidly chemical resistance evolves in agricultural ecosystems.

scholarly journals Stochastic processes drive rapid genomic divergence during experimental range expansions

2019 ◽  
Vol 286 (1900) ◽  
pp. 20190231 ◽  
Author(s):  
Christopher Weiss-Lehman ◽  
Silas Tittes ◽  
Nolan C. Kane ◽  
Ruth A. Hufbauer ◽  
Brett A. Melbourne
Keyword(s):  
De Novo ◽  
Rapid Evolution ◽  
Stochastic Variation ◽  
Genomic Changes ◽  
Neutral Processes ◽  
Standing Variation ◽  
Genomic Divergence ◽  
Expansion Speed ◽  
Edge Populations

Range expansions are crucibles for rapid evolution, acting via both selective and neutral mechanisms. While selection on traits such as dispersal and fecundity may increase expansion speed, neutral mechanisms arising from repeated bottlenecks and genetic drift in edge populations (i.e. gene surfing) could slow spread or make it less predictable. Thus, it is necessary to disentangle the effects of selection from neutral mechanisms to robustly predict expansion dynamics. This is difficult to do with expansions in nature, as replicated expansions are required to distinguish selective and neutral processes in the genome. Using replicated microcosms of the red flour beetle ( Tribolium castaneum ), we identify a robust signature of stochastic, neutral mechanisms in genomic changes arising over only eight generations of expansion and assess the role of standing variation and de novo mutations in driving these changes. Average genetic diversity was reduced within edge populations, but with substantial among-replicate variability in the changes at specific genomic windows. Such variability in genomic changes is consistent with a large role for stochastic, neutral processes. This increased genomic divergence among populations was mirrored by heightened variation in population size and expansion speed, suggesting that stochastic variation in the genome could increase unpredictability of range expansions.

scholarly journals A few stickleback suffice for the transport of alleles to new lakes

2019 ◽  
Author(s):  
Jared Galloway ◽  
William A. Cresko ◽  
Peter Ralph
Keyword(s):  
Gene Flow ◽  
Local Adaptation ◽  
De Novo ◽  
Empirical Studies ◽  
Low Frequency ◽  
Small Fish ◽  
Marine Population ◽  
Standing Variation ◽  
Population Genomic ◽  
Genomic Studies

AbstractThreespine stickleback populations provide a striking example of local adaptation to divergent habitats in populations that are connected by recurrent gene flow. These small fish occur in marine and freshwater habitats throughout the Northern Hemisphere, and in numerous cases the smaller freshwater populations have been established “de novo” from marine colonists. Independently evolved freshwater populations show similar phenotypes that have been shown to derive largely from the same standing genetic variants. Geographic isolation prevents direct migration between the freshwater populations, strongly suggesting that these shared locally adaptive alleles are transported through the marine population. However it is still largely unknown how gene flow, recombination, and selection jointly impact the standing variation that might fuel this adaptation. Here we use individual-based, spatially explicit simulations to determine the levels of gene flow that best match observed patterns of allele sharing among habitats in stickleback. We aim to better understand how gene flow and local adaptation in large metapopulations determine the speed of adaptation and re-use of standing genetic variation. In our simulations we find that repeated adaptation uses a shared set of alleles that are maintained at low frequency by migration-selection balance in oceanic populations. This process occurs over a realistic range of intermediate levels of gene flow that match previous empirical population genomic studies in stickleback. Examining these simulations more deeply reveals how lower levels of gene flow leads to slow, independent adaptation to different habitats, whereas higher levels gene flow leads to significant mutation load – but an increased probability of successful population genomic scans for locally adapted alleles. Surprisingly, we find that the genealogical origins of most freshwater adapted alleles can be traced back to the original generation of marine individuals that colonized the lakes, as opposed to subsequent migrants. These simulations provide deeper context for existing studies of stickleback evolutionary genomics, and guidance for future empirical studies in this model. More broadly, our results support existing theory of local adaptation but extend it by more completely documenting the genealogical history of adaptive alleles in a metapopulation.

scholarly journals Refining the role of de novo protein truncating variants in neurodevelopmental disorders using population reference samples

2016 ◽  
Author(s):  
Jack A. Kosmicki ◽  
Kaitlin E. Samocha ◽  
Daniel P. Howrigan ◽  
Stephan J. Sanders ◽  
Kamil Slowikowski ◽  
...  
Keyword(s):  
Neurodevelopmental Disorders ◽  
De Novo ◽  
Population Based ◽  
Autism Spectrum ◽  
Loss Of Function ◽  
Aggregated Data ◽  
Pathogenic Variants ◽  
Standing Variation ◽  
Reference Samples

AbstractRecent research has uncovered an important role for de novo variation in neurodevelopmental disorders. Using aggregated data from 9246 families with autism spectrum disorder, intellectual disability, or developmental delay, we show ~1/3 of de novo variants are independently observed as standing variation in the Exome Aggregation Consortium’s cohort of 60,706 adults, and these de novo variants do not contribute to neurodevelopmental risk. We further use a loss-of-function (LoF)-intolerance metric, pLI, to identify a subset of LoF-intolerant genes that contain the observed signal of associated de novo protein truncating variants (PTVs) in neurodevelopmental disorders. LoF-intolerant genes also carry a modest excess of inherited PTVs; though the strongest de novo impacted genes contribute little to this, suggesting the excess of inherited risk resides lower-penetrant genes. These findings illustrate the importance of population-based reference cohorts for the interpretation of candidate pathogenic variants, even for analyses of complex diseases and de novo variation.

scholarly journals Selection on growth rate and local adaptation drive genomic adaptation during experimental range expansions in the protist Tetrahymena thermophila

2021 ◽  
Author(s):  
Felix Moerman ◽  
Emanuel A. Fronhofer ◽  
Florian Altermatt ◽  
Andreas Wagner
Keyword(s):  
Gene Flow ◽  
Sexual Reproduction ◽  
Range Expansion ◽  
De Novo ◽  
Tetrahymena Thermophila ◽  
Ph Gradient ◽  
Genetic Changes ◽  
Experimental Range ◽  
Standing Variation ◽  
Genomic Adaptation

AbstractPopulations that expand their range can undergo rapid evolutionary adaptation, which can be aided or hindered by sexual reproduction and gene flow. Little is known about the genomic causes and consequences of such adaptation. We studied genomic adaptation during experimental range expansions of the protist Tetrahymena thermophila in landscapes with a uniform environment or a pH-gradient, both in the presence and absence of gene flow and sexual reproduction. We used pooled genome sequencing to identify genes subject to selection caused by the expanding range and by the pH-gradient. Adaptation to the range expansion affected genes involved in cell divisions and DNA repair, whereas adaptation to the pH gradient additionally affected genes involved in ion balance, and oxidoreductase reactions. These genetic changes may result from selection on growth and adaptation to low pH. Sexual reproduction affected both de novo mutation and standing genetic variation, whereas gene flow and the presence of a pH-gradient affected only standing variation. Sexual reproduction may have aided genetic adaptation during range expansion, but only in the absence of gene flow, which may have swamped expanding populations with maladapted alleles.

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