Biology subjects

Monnahan, P.

Publications and source records attributed to Monnahan, P..

12 recordsLinked to original sources

bioRxiv2023

Kinetochore and ionomic adaptation to whole genome duplication

Transforming genomic and cellular landscapes in a single generation, whole genome duplication (WGD) brings fundamental challenges, but is also associated with diversification. How is WGD tolerated, and what processes commonly evolve to stabilize the resulting polyploid? Here we study this in Cochlearia spp., which have experienced multiple WGDs in the last 300,000 years. We first generate a chromosome-scale genome and sequence 113 individuals from 33 diploid, tetraploid, hexaploid, and outgroup populations. We detect the clearest post-WGD selection signatures in functionally interacting kinetochore components and ion transporters. We structurally model these derived selected alleles, identifying striking WGD-relevant functional variation, and then compare these results to independent recent post-WGD selection in Arabidopsis arenosa and Cardamine amara. Most prominent in these results is genetic evidence of at least four functionally interacting kinetochore complex subunits in adaptation to WGD at the centromere among our very top selective sweep outliers. In addition, some of the same biological processes evolve in all three WGDs, but specific genes recruited are flexible. This points to a polygenic basis for modifying systems that control the kinetochore, meiotic crossover number, DNA repair, ion homeostasis, and cell cycle. Given that DNA management (especially repair) is the most salient category with the strongest selection signal, we speculate that the generation rate of structural genomic variants may be altered by WGD in young polyploids, contributing to their occasionally spectacular adaptability observed across kingdoms. Significance StatementWhole-genome duplication (WGD) occurs in all kingdoms and is linked to adaptation, speciation, domestication, and even cancer outcome. But WGD is a shock to the system, and commonly disrupts cell division due to increased DNA management burden and transformed cell physiology. Nevertheless, the hopeful monster that survives WGD is special, occasionally experiencing runaway success. Why do some thrive but others die? Here we introduce a powerful new model, Cochlearia, which has benefitted from multiple WGDs, and we provide the first genetic evidence of rapid adaptation of functionally interacting components of the cell division machinery, the kinetochore. We also compare which processes and genes evolve to stabilize the new polyploid in three independent cases and highlight common mechanisms.

evolutionary biology↗

bioRxiv2023

Importance of genetic architecture in marker selection decisions for genomic prediction

Breeders commonly use genetic markers to predict the performance of untested individuals as a way to improve the efficiency of breeding programs. These genomic prediction models have almost exclusively used single nucleotide polymorphisms (SNPs) as their source of genetic information, even though other types of markers exist, such as structural variants (SVs). Given that SVs are associated with environmental adaptation and not all of them are in linkage disequilibrium to SNPs, SVs have the potential to bring additional information to multi-environment prediction models that are not captured by SNPs alone. Here, we evaluated different marker types (SNPs and/or SVs) on prediction accuracy across a range of genetic architectures for simulated traits across multiple environments. Our results show that SVs can improve prediction accuracy by up to 19%, but it is highly dependent on the genetic architecture of the trait. Differences in prediction accuracy across marker types were more pronounced for traits with high heritability, high number of QTLs, and SVs as causative variants. In these scenarios, using SV markers resulted in better prediction accuracies than SNP markers, especially when predicting untested genotypes across environments, likely due to more predictors being in linkage disequilibrium with causative variants. The simulations revealed little impact of different effect sizes between SNPs and SVs as causative variants on prediction accuracy. This study demonstrates the importance of knowing the genetic architecture of a trait in deciding what markers and marker types to use in large scale genomic prediction modeling in a breeding program. Key messageWe demonstrate potential for improved multi-environment genomic prediction accuracy using structural variant markers. However, the degree of observed improvement is highly dependent on the genetic architecture of the trait.

plant biology↗

bioRxiv2021

Genetic Architecture of Kernel Compositional Variation in a Maize Diversity Panel

Maize (Zea mays L.) is a multi-purpose row crop grown worldwide, which overtime has often been bred for increased yield at the detriment of lower composition grain quality. Some knowledge of the genetic factors that affect quality traits has been discovered through the study of classical maize mutants. However, much of the underlying genetic architecture controlling these traits and the interaction between these traits remains unknown. To better understand variation that exists for grain compositional traits in maize, we evaluated 501 diverse temperate maize inbred lines in five unique environments and predicted 16 compositional traits (e.g. carbohydrates, protein, starch) based on the output of near-infrared (NIR) spectroscopy. Phenotypic analysis found substantial variation for compositional traits and the majority of variation was explained by genetic and environmental factors. Correlations and trade-offs among traits in different maize types (e.g. dent, sweetcorn, popcorn) were explored and significant differences and correlations were detected. In total, 22.9-71.1% of the phenotypic variation across these traits could be explained using 2,386,666 single nucleotide polymorphism (SNP) markers generated from whole genome resequencing data. A genome-wide association study (GWAS) was conducted using these same markers and found 70 statistically significant loci for 12 compositional traits. This study provides valuable insights in the phenotypic variation and genetic architecture underlying compositional traits that can be used in breeding programs for improving maize grain quality. Core IdeasO_LIUnderstanding kernel compositional variation is important for food grade corn improvement. C_LIO_LIGenetic and environmental factors account for most of the variation in compositional traits. C_LIO_LIA broad range in trait heritabilities was observed across compositional traits. C_LIO_LICompositional trade-offs will be important to consider when conducting multitrait breeding. C_LIO_LICompositional traits are mostly controlled by a large number of small effect loci. C_LI

plant biology↗

bioRxiv2020

Population Level Variation of Transposable Elements in a Maize Diversity Panel

Intact transposable elements (TEs) account for 65% of the maize genome and can impact gene function and regulation. Although TEs comprise the majority of the maize genome and affect important phenotypes, genome wide patterns of TE polymorphisms in maize have only been studied in a handful of maize genotypes, due to the challenging nature of assessing highly repetitive sequences. We implemented a method to use short read sequencing data from 509 diverse inbred lines to classify the presence/absence of 445,418 non-redundant TEs that were previously annotated in four genome assemblies including B73, Mo17, PH207, and W22. Different orders of TEs (i.e. LTRs, Helitrons, TIRs) had different frequency distributions within the population. LTRs with lower LTR similarity were generally more frequent in the population than LTRs with higher LTR similarity, though high frequency insertions with very high LTR similarity were observed. LTR similarity and frequency estimates of nested elements and the outer elements in which they insert revealed that most nesting events occurred very near the timing of the outer element insertion. TEs within genes were at higher frequency than those that were outside of genes and this is particularly true for those not inserted into introns. Many TE insertional polymorphisms observed in this population were tagged by SNP markers. However, there were also 19.9% of the TE polymorphisms that were not well tagged by SNPs (R2 < 0.5) that potentially represent information that has not been well captured in previous SNP based marker-trait association studies. This study provides a population scale genome-wide assessment of TE variation in maize, and provides valuable insight on variation in TEs in maize and factors that contribute to this variation.

plant biology↗

bioRxiv2020

Predicting evolutionary change at the DNA level in a natural Mimulus population

Evolution by natural selection occurs when the frequencies of genetic variants change because individuals differ in Darwinian fitness components such as survival or reproductive success. Differential fitness has been demonstrated in field studies of many organisms, but our ability to quantitatively predict allele frequency changes from fitness measurements remains unclear. Here, we characterize natural selection on millions of Single Nucleotide Polymorphisms (SNPs) across the genome of the annual plant Mimulus guttatus. We use fitness estimates to calibrate population genetic models that effectively predict observed allele frequency changes into the next generation. Hundreds of SNPs experienced "male selection" in 2013 with one allele at each SNP elevated in frequency among successful male gametes relative to the entire population of adults. In the following generation, allele frequencies at these SNPs consistently shifted in the predicted direction. A second year of study revealed that SNPs had effects on both viability and reproductive success with pervasive trade-offs between fitness components. SNPs favored by male selection were, on average, detrimental to survival. These trade-offs (antagonistic pleiotropy and temporal fluctuations in fitness) may be essential to the long-term maintenance of alleles undergoing substantial changes from generation to generation. Despite the challenges of measuring selection in the wild, the strong correlation between predicted and observed allele frequency changes suggests that population genetic models have a much greater role to play in forward-time prediction of evolutionary change. Author summaryFor the last 100 years, population geneticists have been deriving equations for {Delta}p, the change in allele frequency owing to mutation, selection, migration, and genetic drift. Seldom are these equations used directly, to match a prediction for {Delta}p to an observation of {Delta}p. Here, we apply genomic sequencing technologies to samples from natural populations, obtaining millions of observations of {Delta}p. We estimate natural selection on SNPs in a natural population of yellow monkeyflowers and find extensive evidence for selection through differential male success. We use the SNP-specific fitness estimates to calibrate a population genetic model that predicts observed {Delta}p into the next generation. We find that when male selection favored one nucleotide at a SNP, that nucleotide increased in frequency in the next generation. Since neither observed nor predicted {Delta}p are generally large in magnitude, we developed a novel method called "haplotype matching" to improve prediction accuracy. The method leverages intensive whole genome sequencing of a reference panel (187 individuals) to infer sequence-specific selection in thousands of field individuals sequenced at much lower coverage. This method proved essential to accurately predicting {Delta}p in this experiment and further development may facilitate population genetic prediction more generally.

evolutionary biology↗

bioRxiv2020

Convergence and novelty in adaptation to whole genome duplication in three independent polyploids

Convergent evolution is observed broadly across the web of life, but the degree of evolutionary constraint during adaptation of core intracellular processes is not known. High constraint has been assumed for conserved processes, such as cell division and DNA repair, but reports of nimble evolutionary shifts in these processes have confounded this expectation. Whole genome duplication (WGD) necessitates the concerted adjustment of a wide range of fundamental intracellular functions but nevertheless has been repeatedly survived in all kingdoms. Given this repeated adaptation to WGD despite obvious intracellular challenges to core processes such as meiosis, we asked: how do lineages not only survive WGD, but sometimes ultimately thrive? Are the solutions employed constrained or diverse? Here we detect genes and processes under selection following WGD in the Cochlearia species complex by performing a scan for selective sweeps following WGD in a large-scale survey of 73 resequenced individuals from 23 populations across Europe. We then contrast our results from two independent WGDs in Arabidopsis arenosa and Cardamine amara. We find that while WGD does require the adaptation of particular functional processes in all three cases, the specific genes recruited to respond are highly flexible. We also observe evidence of varying degrees of convergence between different cases. Our results point to a polygenic basis for the distributed adaptive systems that control meiotic crossover number, ionomic rewiring, cell cycle control, and nuclear regulation. Given the sheer number of loci under selection post-WGD, we surmise that this polygenicity may explain the general lack of convergence between these species that are ~30 million years diverged. Based on our results, we speculate that adaptive processes themselves - such as the rate of generation of structural genomic variants--may be altered by WGD in nascent autopolyploids, contributing to the occasionally spectacular adaptability of autopolyploids observed across kingdoms.

evolutionary biology↗

bioRxiv2020

Genomic novelty versus convergence in the basis of adaptation to whole genome duplication

Whole genome duplication (WGD) occurs across kingdoms and can promote adaptation. However, a sudden increase in chromosome number, as well as changes in physiology, are traumatic to conserved processes. Previous work in Arabidopsis arenosa revealed a coordinated genomic response to WGD, involving physically interacting meiosis proteins, as well as changes related to cell cycle and ion homeostasis. Here we ask: is this coordinated shift in the same processes repeated in another species following WGD? To answer this, we resequenced and cytologically assessed replicated populations from a diploid/autotetraploid system, Cardamine amara, and test the hypothesis that gene and process-level convergence will be prevalent between these two WGDs adaptation events. Interestingly, we find that gene-level convergence is negligible, with no more in common than would be expected by chance. This was most clear at meiosis-related genes, consistent with our cytological assessment of somewhat lower meiotic stability in C. amara, despite establishment and broad occurrence of the autotetraploid in nature. In contrast, obvious convergence at the level of functional processes, including meiotic cell cycle, chromosome organisation and stress signalling was evident. This indicates that the two autotetraploids survived challenges attendant to WGD via contrasting solutions, modifying different players from similar processes. Overall, this work gives the first insight into the salient adaptations required to cope with a genome-doubled state and brings the first genomic evidence that autopolyploids can utilize multiple trajectories to achieve adaptation to WGD. We speculate that this flexibility increases the likelihood a nascent polyploid overcomes early stringent challenges to later access the spectrum of evolutionary opportunities of polyploidy. Significance statementWhole genome duplication (WGD) is a tremendous mutation and an important evolutionary force. It also presents immediate changes to meiosis and cell physiology that nascent polyploids must overcome to survive. Given the dual facts that WGD adaptation is difficult, but many lineages nevertheless survive WGD, we ask: how constrained are the evolutionary responses to a genome-doubled state? We previously identified candidate genes for WGD adaptation in Arabidopsis arenosa, which has natural diploid and tetraploid variants. Here we test for evolutionary convergence in adaptation to WGD in a species 17 million years distant, Cardamine amara. This work gives the first genomic insight into of how autopolyploids utilize multiple adaptive trajectories to manage a genome-doubled state.

evolutionary biology↗

bioRxiv2019

The effect of autopolyploidy on population genetic signals of hard sweeps

Searching for population genomic signals left behind by positive selection is a major focus of evolutionary biology, particularly as sequencing technologies develop and costs decline. The effect of the number of chromosome copies (i.e. ploidy) on the manifestation of these signals remains an outstanding question, despite a wide appreciation of ploidy being a fundamental parameter governing numerous biological processes. We clarify the principal forces governing the differential manifestation and persistence of the signal of selection by separating the effects of polyploidy on rates of fixation versus rates of diversity (i.e. mutation and recombination) with a set of coalescent simulations. We explore what the major consequences of polyploidy, such as a more localized signal, greater dependence on dominance, and longer persistence of the signal following fixation, mean for within- and across-ploidy inference on the strength and prevalence of selective sweeps. As genomic advances continue to open doors for interrogating natural systems, studies such as this aid our ability to anticipate, interpret, and compare data across ploidy levels.

evolutionary biology↗

bioRxiv2019

Interspecific introgression mediates adaptation to whole genome duplication

Adaptive gene flow is a consequential evolutionary phenomenon across all kingdoms of life. While recognition of widespread gene flow is growing, examples lack of bidirectional gene flow mediating adaptations at specific loci that cooperatively manage core cellular processes. We previously described concerted molecular changes among physically interacting members of the meiotic machinery controlling crossover number and distribution upon adaptation to whole genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that escape from extinction following the trauma of WGD was mediated by adaptive gene flow between A. arenosa and its congener Arabidopsis lyrata. We show that A. lyrata underwent WGD more recently than A. arenosa, indicating that specific pre-adapted alleles donated by A. arenosa underwent selection and rescued the nascent A. lyrata tetraploids from early extinction. At the same time, we detect specific signals of gene flow in the opposite direction at other functionally interacting gene coding loci that display dramatic signatures of selective sweep in both tetraploid species. Cytological analysis shows that A. lyrata tetraploids exhibit similar levels of meiotic stability as A. arenosa tetraploids. Taken together, these data indicate that bidirectional gene flow allowed for an escape from extinction of the young autopolyploids, especially the rare tetraploid A. lyrata, and suggest that the merger of these species is greater than the sum of their parts.

evolutionary biology↗

bioRxiv2018

Pervasive population genomic consequences of genome duplication in Arabidopsis arenosa

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.

evolutionary biology↗

bioRxiv2018

Extreme copy number variation at a tRNA ligase affecting phenology and fitness in yellow monkeyflowers

Copy number variation (CNV) is a major part of the genetic diversity segregating within populations, but remains poorly understood relative to single nucleotide variation. Here, we report on a tRNA ligase gene (Migut.N02091; RLG1a) exhibiting unprecedented, and fitness-relevant, CNV within an annual population of the yellow monkeyflower Mimulus guttatus. RLG1a variation was associated with multiple traits in pooled population sequencing (PoolSeq) scans of phenotypic and phenological cohorts. Resequencing of inbred lines revealed intermediate frequency three-copy variants of RLG1a (trip+; 5/35 = 14%), and trip+ lines exhibited elevated RLG1a expression under multiple conditions. trip+ carriers, in addition to being over-represented in late-flowering and large-flowered PoolSeq populations, flowered later under stressful conditions in a greenhouse experiment (P < 0.05). In wild population samples, we discovered an additional rare RLG1a variant (high+) that carries 250-300 copies of RLG1a totaling [~]5.7Mb (20-40% of a chromosome). In the progeny of a high+ carrier, Mendelian segregation of diagnostic alleles and qPCR-based copy counts indicate that high+ is a single tandem array unlinked from the single copy RLG1a locus. In the wild, high+ carriers had highest fitness in two particularly dry and/or hot years (2015 and 2017; both p < 0.01), while single copy individuals were twice as fecund as either CNV type in a lush year (2016: p < 0.005). Our results demonstrate fluctuating selection on CNVs affecting phenological traits in a wild population, suggest that plant tRNA ligases mediate stress-responsive life-history traits, and introduce a novel system for investigating the molecular mechanisms of gene amplification.

evolutionary biology↗

bioRxiv2017

The genomic architecture of flowering time varies across space and time in Mimulus guttatus

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 method 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. We find appreciable variation in genetic effects on flowering time across both time and space; the greatest differences evident between populations. Structural variants, such as inversions, and genes from multiple flowering time pathways exhibit the strongest associations with flowering time. It is also clear that genotype-by-environment interactions are an important influence on flowering time variation.

genomics↗