David B. Lowry

Michigan State University, Ист-Лансинг, Michigan, United States

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Publications (66)

  • David B. Lowry · Sean Hoban · Joanna L. Kelley · [...] · Andrew Storfer
    [Show abstract] [Hide abstract] ABSTRACT: Understanding how and why populations evolve is of fundamental importance to molecular ecology. RADseq (Restriction site-Associated DNA sequencing), a popular reduced representation method, has ushered in a new era of genome-scale research for assessing population structure, hybridization, demographic history, phylogeography, and migration. RADseq has also been widely used to conduct genome scans to detect loci involved in adaptive divergence among natural populations. Here, we examine the capacity of those RADseq-based genome scan studies to detect loci involved in local adaptation. To understand what proportion of the genome is missed by RADseq studies, we developed a simple model using different numbers of RAD-tags, genome sizes, and extents of linkage disequilibrium (length of haplotype blocks). Under the best case modelling scenario, we found that RADseq using six- or eight- base pair cutting restriction enzymes would fail to sample many regions of the genome, especially for species with short linkage disequilibrium. We then surveyed recent studies that have used RADseq for genome scans and found that that the median density of markers across these studies was 4.08 RAD-tag markers per megabase (1 marker per 245 kilobases). The length of linkage disequilibrium for many species is one to three orders of magnitude less than density of the typical recent RADseq study. Thus, we conclude that genome scans based on RADseq data alone, while useful for studies of neutral genetic variation and genetic population structure, will likely miss many loci under selection in studies of local adaptation. This article is protected by copyright. All rights reserved.
    Article · Nov 2016 · Molecular Ecology Resources
  • David B Lowry · Sean Hoban · Joanna L Kelley · [...] · Andrew Storfer
    [Show abstract] [Hide abstract] ABSTRACT: Understanding how and why populations evolve is of fundamental importance to molecular ecology. RADseq (Restriction site-Associated DNA sequencing), a popular reduced representation method, has ushered in a new era of genome-scale research for assessing population structure, hybridization, demographic history, phylogeography, and migration. RADseq has also been widely used to conduct genome scans to detect loci involved in adaptive divergence among natural populations. Here, we examine the capacity of those RADseq-based genome scan studies to detect loci involved in local adaptation. To understand what proportion of the genome is missed by RADseq studies, we developed a simple model using different numbers of RAD-tags, genome sizes, and extents of linkage disequilibrium (length of haplotype blocks). We then surveyed recent studies that have used RADseq for genome scans and found that that the median density of RADseq markers across these studies was one marker per 3.96 megabases. Given that the length of linkage disequilibrium is often orders of magnitude less than a megabase, we conclude that genome scans based on RADseq data alone are unlikely to advance our understanding of molecular ecology or evolutionary genetics for most systems. This article is protected by copyright. All rights reserved.
    Article · Sep 2016 · Molecular Ecology Resources
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    Elizabeth R Milano · David B Lowry · Thomas E Juenger
    [Show abstract] [Hide abstract] ABSTRACT: The evolution of locally adapted ecotypes is a common phenomenon that generates diversity within plant species. However, we know surprisingly little about the genetic mechanisms underlying the locally adapted traits involved in ecotype formation. The genetic architecture underlying locally adapted traits dictates how an organism will respond to environmental selection pressures and has major implications for evolutionary ecology, conservation, and crop breeding. To understand the genetic architecture underlying the divergence of switchgrass (Panicum virgatum) ecotypes, we constructed a genetic mapping population through a four-way outbred cross between two northern upland and two southern lowland accessions. Trait segregation in this mapping population was largely consistent with multiple independent loci controlling the suite of traits that characterizes ecotype divergence. We assembled a joint linkage map using ddRADseq and mapped quantitative trait loci (QTL) for traits that are divergent between ecotypes, including flowering time, plant size, physiological processes, and disease resistance. Overall, we found that most QTL had small to intermediate effects. While we identified colocalizing QTLs for multiple traits, we did not find any large-effect QTLs that clearly controlled multiple traits through pleiotropy or tight physical linkage. These results indicate that ecologically important traits in switchgrass have a complex genetic basis and that similar loci may underlie divergence across the geographic range of the ecotypes.
    Full-text available · Article · Sep 2016 · G3-Genes Genomes Genetics
  • Elizabeth R. Milano · David B. Lowry · Thomas E. Juenger
    File available · Data · Sep 2016
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    [Show abstract] [Hide abstract] ABSTRACT: Uncovering the genetic and evolutionary basis of local adaptation is a major focus of evolutionary biology. The recent development of cost-effective methods for obtaining high-quality genome-scale data makes it possible to identify some of the loci responsible for adaptive differences among populations. Two basic approaches for identifying putatively locally adaptive loci have been developed and are broadly used: one that identifies loci with unusually high genetic differentiation among populations (differentiation outlier methods) and one that searches for correlations between local population allele frequencies and local environments (genetic-environment association methods). Here, we review the promises and challenges of these genome scan methods, including correcting for the confounding influence of a species' demographic history, biases caused by missing aspects of the genome, matching scales of environmental data with population structure, and other statistical considerations. In each case, we make suggestions for best practices for maximizing the accuracy and efficiency of genome scans to detect the underlying genetic basis of local adaptation. With attention to their current limitations, genome scan methods can be an important tool in finding the genetic basis of adaptive evolutionary change.
    Full-text available · Article · Aug 2016 · The American Naturalist
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    Samuel H. Taylor · David B. Lowry · Michael J. Aspinwall · [...] · Thomas E. Juenger
    [Show abstract] [Hide abstract] ABSTRACT: Switchgrass is a key component of plans to develop sustainable cellulosic ethanol production for bioenergy in the USA. We sought quantitative trait loci (QTL) for leaf structure and function, using the Albany full-sib mapping population, an F1 derived from lowland tetraploid parents. We also assessed both genotype × environment interactions (G×E) in response to drought and spatial trends within experimental plots, using the mapping population and check clones drawn from the parent cultivars. Phenotypes for leaf structure and physiological performance were determined under well-watered conditions in two consecutive years, and we applied drought to one of two replicates to test for G×E. Phenotypes for check clones varied with location in our plot and were impacted by drought, but there was limited evidence of G×E except in quantum yield (ΦPSII). Phenotypes of Albany were also influenced by plant location within our plot, and after correcting for experimental design factors and spatial effects, we detected QTL for leaf size, tissue density (LMA), and stomatal conductance (g s ). Clear evidence of G×E was detected at a QTL for intrinsic water use efficiency (iWUE) that was expressed only under drought. Loci influencing physiological traits had small additive effects, showed complex patterns of heritability, and did not co-localize with QTL for morphological traits. These insights into the genetic architecture of leaf structure and function set the stage for consideration of leaf physiological phenotypes as a component of switchgrass improvement for bioenergy purposes.
    Full-text available · Article · Jun 2016 · BioEnergy Research
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    [Show abstract] [Hide abstract] ABSTRACT: Identifying the physiological and genetic basis of stress tolerance in plants has proven to be critical to understanding adaptation in both agricultural and natural systems. However, many discoveries were initially made in the controlled conditions of greenhouses or laboratories, not in the field. To test the comparability of drought responses across field and greenhouse environments, we undertook three independent experiments using the switchgrass reference genotype Alamo AP13. We analyzed physiological and gene-expression variation across four locations, two sampling times and three years. Relatively similar physiological responses and expression coefficients of variation across experiments masked highly dissimilar gene expression responses to drought. Critically, a drought experiment utilizing small pots in the greenhouse elicited nearly identical physiological changes as an experiment conducted in the field, but an order of magnitude more differentially expressed genes. However, we were able to define a suite of several hundred genes that were differentially expressed in each experiment. This list was strongly enriched in photosynthesis, water status and reactive oxygen species responsive genes. The strong across-experiment correlations between physiological plasticity-but not differential gene expression-highlight the complex and diverse genetic mechanisms that can produce phenotypically similar responses to various soil water deficits.
    Full-text available · Article · May 2016 · Plant physiology
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    [Show abstract] [Hide abstract] ABSTRACT: Aims Variation in precipitation strongly influences plant growth, species distributions, and genetic diversity. Intraspecific variation in phenotypic plasticity, the ability of a genotype to alter its growth, morphology or physiology in response to the environment, could influence species responses to changing precipitation and climate change. Despite this, the patterns and mechanisms of intraspecific variation in plasticity to variable precipitation, and the degree to which genotype responses to precipitation are influenced by variation in edaphic conditions, remain poorly understood. Thus, we determined whether genotypes of a widespread C4 grass (Panicum virgatum L., switchgrass) varied in aboveground productivity in response to changes in precipitation, and if site edaphic conditions modified genotype aboveground productivity responses to precipitation. We also determined if genotype productivity responses to precipitation are related to plasticity in underlying growth and phenological traits. Methods Nine P. virgatum genotypes originating from an aridity gradient were grown under four treatments spanning the 10th to the 90th percentiles of annual precipitation at two sites in central Texas; one site with deep, fine-textured soils and another site with shallow, coarse-textured soils. We measured volumetric soil water content (VWC), aboveground net primary productivity (ANPP), tiller production (tiller number), average tiller mass, canopy height, leaf area index (LAI), and flowering time on all plants at both sites and examined genotype responses to changes in precipitation. Important Findings Across precipitation treatments, VWC was 39% lower and more variable at the site with shallow, coarse-textured soils compared to the site with deep, fine-textured soils. ANPP averaged across genotypes and precipitation treatments was also 103% higher at the site with deep, fine-textured soils relative to the site with shallow, coarse-textured soils, indicating substantial differences in site water limitation. Where site water limitation was higher, ANPP of most genotypes increased with increasing precipitation. Where site water limitation was less, genotypes expressed variable plasticity in response to precipitation, from no change to almost a 5-fold increase in ANPP with increasing precipitation. Genotype ANPP increased with greater tiller mass, LAI, and later flowering time at both sites, but not with tiller number at either site. Genotype ANPP plasticity increased with genotype tiller mass and LAI plasticity at the site with deep, fine-textured soils, and only with genotype tiller mass plasticity at the site with shallow, coarse textured soils. Thus, variation in genotype ANPP plasticity was explained primarily by variation in tiller and leaf growth. Genotype ANPP plasticity was not associated with temperature or aridity at the genotype’s origin. Edaphic factors such as soil depth and texture may alter genotype ANPP responses to precipitation, and the underlying growth traits contributing to the ANPP response. Thus, edaphic factors may contribute to spatial variation in genotype performance and success under altered precipitation.
    Full-text available · Article · Apr 2016 · Journal of Plant Ecology
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    John T. Lovell · Scott Schwartz · David B. Lowry · [...] · Thomas E. Juenger
    [Show abstract] [Hide abstract] ABSTRACT: Climatic adaptation is an example of a genotype-by-environment interaction (G×E) of fitness. Selection upon gene expression regulatory variation can contribute to adaptive phenotypic diversity; however, surprisingly few studies have examined how genome-wide patterns of gene expression G×E are manifested in response to environmental stress and other selective agents that cause climatic adaptation. Here, we characterize drought-responsive expression divergence between upland (drought-adapted) and lowland (mesic) ecotypes of the perennial C4 grass, Panicum hallii, in natural field conditions. Overall, we find that cis-regulatory elements contributed to gene expression divergence across 47% of genes, 7.2% of which exhibit drought-responsive G×E. While less well-represented, we observe 1294 genes (7.8%) with trans effects. Trans-by-environment interactions are weaker and much less common than cis G×E, occurring in only 0.7% of trans-regulated genes. Finally, gene expression heterosis is highly enriched in expression phenotypes with significant G×E. As such, modes of inheritance that drive heterosis, such as dominance or overdominance, may be common among G×E genes. Interestingly, motifs specific to drought-responsive transcription factors are highly enriched in the promoters of genes exhibiting G×E and trans regulation, indicating that expression G×E and heterosis may result from the evolution of transcription factors or their binding sites. P. hallii serves as the genomic model for its close relative and emerging biofuel crop, switchgrass (Panicum virgatum). Accordingly, the results here not only aid in the discovery of the genetic mechanisms that underlie local adaptation but also provide a foundation to improve switchgrass yield under water-limited conditions.
    Full-text available · Article · Mar 2016 · Genome Research
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    [Show abstract] [Hide abstract] ABSTRACT: Gene flow may influence the formation of species range limits, yet little is known about the patterns of gene flow with respect to environmental gradients or proximity to range limits. With rapid environmental change it is especially important to understand patterns of gene flow to inform conservation efforts. Here we investigate the species range of the selfing, annual plant, Mimulus laciniatus, in the California Sierra Nevada. We assessed genetic variation, gene flow, and population abundance across the entire elevation-based climate range. Contrary to expectations, within-population plant density increased towards both climate limits. Mean genetic diversity of edge populations was equivalent to central populations, however all edge populations exhibited less genetic diversity than neighboring interior populations. Genetic differentiation was fairly consistent and moderate among all populations and no directional signals of contemporary gene flow were detected between central and peripheral elevations. Elevation-driven gene flow (isolation by environment), but not isolation by distance was found across the species range. These findings were the same towards high- and low-elevation range limits and were inconsistent with two common center-edge hypotheses invoked for the formation of species range limits: 1) decreasing habitat quality and population size; 2) swamping gene flow from large, central populations. This pattern demonstrates that climate, but not center-edge dynamics, is an important range-wide factor structuring M. laciniatus populations. To our knowledge this is the first empirical study to relate environmental patterns of gene flow to range limits hypotheses. Similar investigations across a wide variety of taxa and life histories are needed. This article is protected by copyright. All rights reserved.
    Full-text available · Article · Jan 2016 · Molecular Ecology
  • David B. Lowry
    Article · Jul 2015 · Rhodora
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    David B Lowry · Samuel H Taylor · Jason Bonnette · [...] · Thomas E Juenger
    [Show abstract] [Hide abstract] ABSTRACT: Genetic and genomic resources have recently been developed for the bioenergy crop switchgrass (Panicum virgatum). Despite these advances, little research has been focused on identifying genetic loci involved in natural variation of important bioenergy traits, including biomass. Quantitative trait locus (QTL) mapping is typically used to discover loci that contribute to trait variation. Once identified, QTLs can be used to improve agronomically important traits through marker-assisted selection. In this study, we conducted QTL mapping in Austin, TX, USA, with a full-sib mapping population derived from a cross between tetraploid clones of two major switchgrass cultivars (Alamo-A4 and Kanlow-K5). We observed significant among-genotype variation for the vast majority of growth, morphological, and phenological traits measured on the mapping population. Overall, we discovered 27 significant QTLs across 23 traits. QTLs for biomass production colocalized on linkage group 9b across years, as well as with a major biomass QTL discovered in another recent switchgrass QTL study. The experiment was conducted under a rainout shelter, which allowed us to examine the effects of differential irrigation on trait values. We found very minimal effects of the reduced watering treatment on traits, with no significant effect on biomass production. Overall, the results of our study set the stage for future crop improvement through marker-assisted selection breeding.
    Full-text available · Article · Jun 2015 · BioEnergy Research
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    John T Lovell · Jack L Mullen · David B Lowry · [...] · John K McKay
    [Show abstract] [Hide abstract] ABSTRACT: Soil water availability represents one of the most important selective agents for plants in nature and the single greatest abiotic determinant of agricultural productivity, yet the genetic bases of drought acclimation responses remain poorly understood. Here, we developed a systems-genetic approach to characterize quantitative trait loci (QTLs), physiological traits and genes that affect responses to soil moisture deficit in the TSUxKAS mapping population of Arabidopsis thaliana. To determine the effects of candidate genes underlying QTLs, we analyzed gene expression as a covariate within the QTL model in an effort to mechanistically link markers, RNA expression, and the phenotype. This strategy produced ranked lists of candidate genes for several drought-associated traits, including water use efficiency, growth, abscisic acid concentration (ABA), and proline concentration. As a proof of concept, we recovered known causal loci for several QTLs. For other traits, including ABA, we identified novel loci not previously associated with drought. Furthermore, we documented natural variation at two key steps in proline metabolism and demonstrated that the mitochondrial genome differentially affects genomic QTLs to influence proline accumulation. These findings demonstrate that linking genome, transcriptome, and phenotype data holds great promise to extend the utility of genetic mapping, even when QTL effects are modest or complex. © 2015 American Society of Plant Biologists. All rights reserved.
    Full-text available · Article · Apr 2015 · The Plant Cell
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    [Show abstract] [Hide abstract] ABSTRACT: Evolutionary biology is in an exciting era, in which powerful genomic tools make accessible the answers to long-standing questions about variation, adaptation, and speciation. The availability of a suite of genomic resources, a shared knowledge-base, and a long history of study have made the phenotypically diverse plant genus Mimulus an important system for understanding evolutionary and ecological processes. An international Mimulus Research Meeting was held at Duke University in June 2014 to discuss developments in evolutionary and ecological genetic studies in Mimulus. Here, we report major recent discoveries presented at the meeting that use genomic approaches to advance our understanding of three major themes: the parallel genetic basis of adaptation; the ecological genomics of speciation; and the evolutionary significance of structural genetic variation. We also suggest future research directions for studies of Mimulus and highlight challenges faced when developing new evolutionary and ecological model systems. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Full-text available · Article · Apr 2015 · Molecular Ecology
  • David B Lowry · Kyle Hernandez · Samuel H Taylor · [...] · Thomas E Juenger
    [Show abstract] [Hide abstract] ABSTRACT: Summary of Illumina libraries used in the preliminary Meraculous Panicum hallii assembly Table S2 R/qtl input file for QTL mapping of morphological traits Table S3 R/qtl input file for QTL mapping of physiological traits
    File available · Data · Sep 2014
  • Data: Fig S1
    David B Lowry · Kyle Hernandez · Samuel H Taylor · [...] · Thomas E Juenger
    [Show abstract] [Hide abstract] ABSTRACT: Flowchart of the pipeline for mapping and SNP calling of RAD-tag markers for the FIL2 × HAL2 hybrid F2 mapping population of Panicum hallii. Fig. S2 Flowchart of the pipeline for synteny analysis between the Panicum hallii linkage map and the genome of foxtail millet (Setaria italica). Fig. S3 Histograms of phenotypic variation for morphological traits in the F2 hybrid population of Panicum hallii. Fig. S4 Histograms of phenotypic variation for physiological traits in the F2 hybrid population of Panicum hallii. Fig. S5 Plot of recombination fractions across the Panicum hallii FIL2 × HAL2 genetic map. Methods S1 Supplementary methods.
    File available · Data · Sep 2014
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    David B. Lowry · Kyle Hernandez · Samuel H. Taylor · [...] · Thomas E. Juenger
    [Show abstract] [Hide abstract] ABSTRACT: The process of plant speciation often involves the evolution of divergent ecotypes in response to differences in soil water availability between habitats. While the same set of traits is frequently associated with xeric/mesic ecotype divergence, it is unknown whether those traits evolve independently or if they evolve in tandem as a result of genetic colocalization either by pleiotropy or genetic linkage. The self-fertilizing C4 grass species Panicum hallii includes two major ecotypes found in xeric (var. hallii) or mesic (var. filipes) habitats. We constructed the first linkage map for P. hallii by genotyping a reduced representation genomic library of an F2 population derived from an intercross of var. hallii and filipes. We then evaluated the genetic architecture of divergence between these ecotypes through quantitative trait locus (QTL) mapping. Overall, we mapped QTLs for nine morphological traits that are involved in the divergence between the ecotypes. QTLs for five key ecotype-differentiating traits all colocalized to the same region of linkage group five. Leaf physiological traits were less divergent between ecotypes, but we still mapped five physiological QTLs. We also discovered a two-locus Dobzhansky–Muller hybrid incompatibility. Our study suggests that ecotype-differentiating traits may evolve in tandem as a result of genetic colocalization.
    Full-text available · Article · Sep 2014 · New Phytologist
  • Eli Meyer · Michael J Aspinwall · David Bryant Lowry · [...] · Thomas E Juenger
    File available · Data · Aug 2014
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    Eli Meyer · Michael J Aspinwall · David Bryant Lowry · [...] · Thomas E Juenger
    [Show abstract] [Hide abstract] ABSTRACT: Background In light of the changes in precipitation and soil water availability expected with climate change, understanding the mechanisms underlying plant responses to water deficit is essential. Toward that end we have conducted an integrative analysis of responses to drought stress in the perennial C4 grass and biofuel crop, Panicum virgatum (switchgrass). Responses to soil drying and re-watering were measured at transcriptional, physiological, and metabolomic levels. To assess the interaction of soil moisture with diel light: dark cycles, we profiled gene expression in drought and control treatments under pre-dawn and mid-day conditions. Results Soil drying resulted in reduced leaf water potential, gas exchange, and chlorophyll fluorescence along with differential expression of a large fraction of the transcriptome (37%). Many transcripts responded differently depending on time of day (e.g. up-regulation pre-dawn and down-regulation mid-day). Genes associated with C4 photosynthesis were down-regulated during drought, while C4 metabolic intermediates accumulated. Rapid changes in gene expression were observed during recovery from drought, along with increased water use efficiency and chlorophyll fluorescence. Conclusions Our findings demonstrate that drought responsive gene expression depends strongly on time of day and that gene expression is extensively modified during the first few hours of drought recovery. Analysis of covariation in gene expression, metabolite abundance, and physiology among plants revealed non-linear relationships that suggest critical thresholds in drought stress responses. Future studies may benefit from evaluating these thresholds among diverse accessions of switchgrass and other C4 grasses. Electronic supplementary material The online version of this article (doi:10.1186/1471-2164-15-527) contains supplementary material, which is available to authorized users.
    Full-text available · Article · Jun 2014 · BMC Genomics
  • Jesse R. Lasky · David L. Des Marais · David B. Lowry · [...] · Thomas E. Juenger
    File available · Data · May 2014