David B Lowry

University of Texas at Austin, Austin, Texas, United States

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Publications (24)124.3 Total impact

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    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.
    New Phytologist 09/2014; · 6.74 Impact Factor
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    ABSTRACT: Gene expression varies widely in natural populations, yet the proximate and ultimate causes of this variation are poorly known. Understanding how variation in gene expression affects abiotic stress tolerance, fitness, and adaptation is central to the field of evolutionary genetics. We tested the hypothesis that genes with natural genetic variation in their expression responses to abiotic stress are likely to be involved in local adaptation to climate in Arabidopsis thaliana. Specifically, we compared genes with consistent expression responses to environmental stress (expression stress responsive, “eSR”) to genes with genetically variable responses to abiotic stress (expression genotype-by-environment interaction, “eGEI”). We found that on average genes that exhibited eGEI in response to drought or cold had greater polymorphism in promoter regions and stronger associations with climate than eSR genes or genomic controls. We also found that transcription factor binding sites known to respond to environmental stressors, especially abscisic acid responsive elements, showed significantly higher polymorphism in drought eGEI genes in comparison to eSR genes. By contrast, eSR genes tended to exhibit relatively greater pairwise haplotype sharing, lower promoter diversity, and fewer non-synonymous polymorphisms, suggesting purifying selection or selective sweeps. Our results indicate that cis-regulatory evolution and genetic variation in stress responsive gene expression may be important mechanisms of local adaptation to climatic selective gradients.
    Molecular Biology and Evolution 05/2014; · 10.35 Impact Factor
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    ABSTRACT: 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 favorable 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.This article is protected by copyright. All rights reserved.
    Molecular Ecology 05/2014; · 6.28 Impact Factor
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    ABSTRACT: Abstract Determining the patterns and mechanisms of natural selection in the wild is of fundamental importance to understanding the differentiation of populations and the evolution of new species. However, it is often unknown the extent to which adaptive genetic variation is distributed among ecotypes between distinct habitats versus along large-scale geographic environmental gradients, such as those that track latitude. Classic studies of selection in the wild in switchgrass, Panicum virgatum, tested for adaptation at both of these levels of natural variation. Here we review what these field experiments and modern agronomic field trials have taught us about natural variation and selection at both the ecotype and environmental gradient levels in P. virgatum. With recent genome sequencing efforts in P. virgatum, it is poised to become an excellent system for understanding the adaptation of grassland species across the eastern half of North America. The identification of genetic loci involved in different types of adaptations will help to understand the evolutionary mechanisms of diversification within P. virgatum and provide useful information for the breeding of high-yielding cultivars for different ecoregions.
    The American Naturalist 05/2014; 183(5):682-92. · 4.55 Impact Factor
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    ABSTRACT: 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.
    BMC genomics. 01/2014; 15:527.
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    ABSTRACT: The regulation of gene expression is crucial for an organism's development and response to stress, and an understanding of the evolution of gene expression is of fundamental importance to basic and applied biology. To improve this understanding, we conducted expression quantitative trait locus (eQTL) mapping in the Tsu-1 (Tsushima, Japan) × Kas-1 (Kashmir, India) recombinant inbred line population of Arabidopsis thaliana across soil drying treatments. We then used genome resequencing data to evaluate whether genomic features (promoter polymorphism, recombination rate, gene length, and gene density) are associated with genes responding to the environment (E) or with genes with genetic variation (G) in gene expression in the form of eQTLs. We identified thousands of genes that responded to soil drying and hundreds of main-effect eQTLs. However, we identified very few statistically significant eQTLs that interacted with the soil drying treatment (GxE eQTL). Analysis of genome resequencing data revealed associations of several genomic features with G and E genes. In general, E genes had lower promoter diversity and local recombination rates. By contrast, genes with eQTLs (G) had significantly greater promoter diversity and were located in genomic regions with higher recombination. These results suggest that genomic architecture may play an important a role in the evolution of gene expression.
    The Plant Cell 09/2013; · 9.25 Impact Factor
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    ABSTRACT: Examining intraspecific variation in growth and function in relation to climate may provide insight into physiological evolution and adaptation, and is important for predicting species responses to climate change. Under common garden conditions, we grew nine genotypes of the C4 species Panicum virgatum originating from different temperature and precipitation environments. We hypothesized that genotype productivity, morphology and physiological traits would be correlated with climate of origin, and a suite of adaptive traits would show high broad-sense heritability (H(2) ). Genotype productivity and flowering time increased and decreased, respectively, with home-climate temperature, and home-climate temperature was correlated with genotypic differences in a syndrome of morphological and physiological traits. Genotype leaf and tiller size, leaf lamina thickness, leaf mass per area (LMA) and C : N ratios increased with home-climate temperature, whereas leaf nitrogen per unit mass (Nm ) and chlorophyll (Chl) decreased with home-climate temperature. Trait variation was largely explained by genotypic differences (H(2) = 0.33-0.85). Our results provide new insight into the role of climate in driving functional trait coordination, local adaptation and genetic divergence within species. These results emphasize the importance of considering intraspecific variation in future climate change scenarios.
    New Phytologist 05/2013; · 6.74 Impact Factor
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    ABSTRACT: • Premise of study: Understanding the relationship between climate, adaptation, and population structure is of fundamental importance to botanists because these factors are crucial for the evolution of biodiversity and the response of species to future climate change. Panicum hallii is an emerging model system for perennial grass and bioenergy research, yet very little is known about the relationship between climate and population structure in this system. • Methods: We analyzed geographic population differentiation across 39 populations of P. hallii along a longitudinal transect from the savannas of central Texas through the deserts of Arizona and New Mexico. A combination of morphological and genetic (microsatellite) analysis was used to explore patterns of population structure. • Key results: We found strong differentiation between high elevation western desert populations and lower elevation eastern populations of P. hallii, with a pronounced break in structure occurring in western Texas. In addition, we confirmed that there are high levels of morphological and genetic structure between previous recognized varieties (var. hallii and var. filipes) within this species. • Conclusions: The results of this study suggest that patterns of population structure within P. hallii may be driven by climatic variation over space. Overall, this study lays the groundwork for future studies on the genetics of local adaptation and reproductive isolation in this system.
    American Journal of Botany 03/2013; 100(3):592-601. · 2.59 Impact Factor
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    ABSTRACT: Most species are superbly and intricately adapted to the environments in which they live. Adaptive evolution by natural selection is the primary force shaping biological diversity. Differences between closely related species in ecologically selected characters such as habitat preference, reproductive timing, courtship behavior, or pollinator attraction may prevent interbreeding in nature, causing reproductive isolation. But does ecological adaptation cause reproductive incompatibilities such as hybrid sterility or lethality? Although several genes causing hybrid incompatibilities have been identified, there is intense debate over whether the genes that contribute to ecological adaptations also cause hybrid incompatibilities. Thirty years ago, a genetic study of local adaptation to copper mine soils in the wildflower identified a locus that appeared to cause copper tolerance and hybrid lethality in crosses to other populations. But do copper tolerance and hybrid lethality have the same molecular genetic basis? Here we show, using high-resolution genome mapping, that copper tolerance and hybrid lethality are not caused by the same gene but are in fact separately controlled by two tightly linked loci. We further show that selection on the copper tolerance locus indirectly caused the hybrid incompatibility allele to go to high frequency in the copper mine population because of hitchhiking. Our results provide a new twist on Darwin's original supposition that hybrid incompatibilities evolve as an incidental by-product of ordinary adaptation to the environment.
    PLoS Biology 02/2013; 11(2):e1001497. · 12.69 Impact Factor
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    David B Lowry
    New Phytologist 06/2012; 194(4):888-90. · 6.74 Impact Factor
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    ABSTRACT: • Premise of the study: We developed microsatellites for Panicum hallii for studies of gene flow, population structure, breeding experiments, and genetic mapping. • Methods and Results: Next-generation (454) genomic sequence data were used to design markers. Eighteen robust markers were discovered, 15 of which were polymorphic across six accessions of P. hallii var. hallii. Fourteen of the markers cross-amplified in a P. capillare accession. For the 15 polymorphic markers, the total number of alleles per locus ranged from two to 26 (mean: 11.0) across six populations (11-19 individuals per population). Observed heterozygosity (mean: 0.031) was 13.7 times lower than the expected heterozygosity (mean: 0.426). • Conclusions: The deficit of heterozygous individuals is consistent with P. hallii having a high rate of self-fertilization. These markers will be useful for studies in P. hallii and related species.
    American Journal of Botany 03/2012; 99(3):e114-6. · 2.59 Impact Factor
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    DAVID B. LOWRY
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    ABSTRACT: Recent interest in the role of ecology in species formation has led to renewed discussion of the stages in the process of speciation. Although attempts to classify the stages in the process of species formation date back at least as far as Alfred Russel Wallace, one of the most intense debates on the subject occurred among botanists during the mid‐20th Century. The present review outlines the progression of the historical debate about stages in the evolution of species, which was instigated by the genecological classification scheme of Göte Turesson in the 1920s, championed in the mid‐century by Jens Clausen, and then brought under harsh scrutiny by many in the 1960s and 1970s. At the heart of the controversy is the question of whether speciation occurs rapidly on a local scale or gradually through the formation of geographically widespread ecotypes that evolve as precursors to species. A corollary to this debate is the question of whether speciation is reversible and, if so, how does it become irreversible? A third wave of interest in stages in the process of speciation is currently underway, thus making a modern historical narrative of the debate important. Both contemporary and past evolutionary biologists have argued that viewing speciation as being composed of stages can free researchers from concerns over species definitions and focus attention on the mechanisms involved in the process. How speciation becomes irreversible and whether ecogeographically isolated ecotypes are integral to this process remain as important unresolved issues. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 241–257.
    Biological Journal of the Linnean Society 01/2012; 106(2). · 2.41 Impact Factor
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    ABSTRACT: Natural variation in the regulation of the accumulation of mineral nutrients and trace elements in plant tissues is crucial to plant metabolism, development, and survival across different habitats. Studies of the genetic basis of natural variation in nutrient metabolism have been facilitated by the development of ionomics. Ionomics is a functional genomic approach for the identification of the genes and gene networks that regulate the elemental composition, or ionome, of an organism. In this study, we evaluated the genetic basis of divergence in elemental composition between an inland annual and a coastal perennial accession of Mimulus guttatus using a recombinant inbred line (RIL) mapping population. Out of 20 elements evaluated, Mo and Cd were the most divergent in accumulation between the two accessions and were highly genetically correlated in the RILs across two replicated experiments. We discovered two major quantitative trait loci (QTL) for Mo accumulation, the largest of which consistently colocalized with a QTL for Cd accumulation. Interestingly, both Mo QTLs also colocalized with the two M. guttatus homologues of MOT1, the only known plant transporter to be involved in natural variation in molybdate uptake.
    PLoS ONE 01/2012; 7(1):e30730. · 3.53 Impact Factor
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    ABSTRACT: • Premise of study: Botanists have long been interested in the reasons for genetic variation among individuals, populations, and species of plants. The anthocyanin pathway is ideal for studying the evolution of such phenotypic variation. • Methods: We used a combination of quantitative trait loci mapping and association studies to understand the genetic basis of variation in five anthocyanin phenotypes including calyx, corolla, and leaf coloration patterns that vary within and among populations of Mimulus guttatus. We then examined what genes might be responsible for this phenotypic variation and whether one of the traits, calyx spotting, is randomly distributed across the geographic range of the species. • Key results: All five phenotypes in M. guttatus were primarily controlled by the same major locus (PLA1), which contains a tandem array of three R2R3-MYB genes known to be involved in the evolution of flower color in a related species of Mimulus. Calyx spotting was nonrandomly distributed across the range of M. guttatus and correlated with multiple climate variables. • Conclusions: The results of this study suggest that variation in R2R3-MYB genes is the primary cause of potentially important anthocyanin phenotypic variation within and among populations of M. guttatus, a finding consistent with recent theoretical and empirical research on flower color evolution.
    American Journal of Botany 12/2011; 99(1):82-91. · 2.59 Impact Factor
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    David B Lowry
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    ABSTRACT: Tremendous advances in genetic and genomic techniques have resulted in the capacity to identify genes involved in adaptive evolution across numerous biological systems. One of the next major steps in evolutionary biology will be to determine how landscape-level geographical and environmental features are involved in the distribution of this functional adaptive genetic variation. Here, I outline how an emerging synthesis of multiple disciplines has and will continue to facilitate a deeper understanding of the ways in which heterogeneity of the natural landscapes mould the genomes of organisms.
    Biology letters 08/2010; 6(4):502-4. · 3.35 Impact Factor
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    M C Hall, D B Lowry, J H Willis
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    ABSTRACT: Local adaptation is considered to be the result of fitness trade-offs for particular phenotypes across different habitats. However, it is unclear whether such phenotypic trade-offs exist at the level of individual genetic loci. Local adaptation could arise from trade-offs of alternative alleles at individual loci or by complementary sets of loci with different fitness effects of alleles in one habitat but selective neutrality in the alternative habitat. To evaluate the genome-wide basis of local adaptation, we performed a field-based quantitative trait locus (QTL) mapping experiment on recombinant inbred lines (RILs) created from coastal perennial and inland annual races of the yellow monkeyflower (Mimulus guttatus) grown reciprocally in native parental habitats. Overall, we detected 19 QTLs affecting one or more of 16 traits measured in two environments, most of small effect. We identified 15 additional QTL effects at two previously identified candidate QTLs [DIVERGENCE (DIV)]. Significant QTL by environment interactions were detected at the DIV loci, which was largely attributable to genotypic differences at a single field site. We found no detectable evidence for trade-offs for any one component of fitness, although DIV2 showed a trade-off involving different fitness traits between sites, suggesting that local adaptation is largely controlled by non-overlapping loci. This is surprising for an outcrosser, implying that reduced gene flow prevents the evolution of individuals adapted to multiple environments. We also determined that native genotypes were not uniformly adaptive, possibly reflecting fixed mutational load in one of the populations.
    Molecular Ecology 07/2010; 19(13):2739-53. · 6.28 Impact Factor
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    David B Lowry, John H Willis
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    ABSTRACT: The role of chromosomal inversions in adaptation and speciation is controversial. Historically, inversions were thought to contribute to these processes either by directly causing hybrid sterility or by facilitating the maintenance of co-adapted gene complexes. Because inversions suppress recombination when heterozygous, a recently proposed local adaptation mechanism predicts that they will spread if they capture alleles at multiple loci involved in divergent adaptation to contrasting environments. Many empirical studies have found inversion polymorphisms linked to putatively adaptive phenotypes or distributed along environmental clines. However, direct involvement of an inversion in local adaptation and consequent ecological reproductive isolation has not to our knowledge been demonstrated in nature. In this study, we discovered that a chromosomal inversion polymorphism is geographically widespread, and we test the extent to which it contributes to adaptation and reproductive isolation under natural field conditions. Replicated crosses between the prezygotically reproductively isolated annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus, revealed that alternative chromosomal inversion arrangements are associated with life-history divergence over thousands of kilometers across North America. The inversion polymorphism affected adaptive flowering time divergence and other morphological traits in all replicated crosses between four pairs of annual and perennial populations. To determine if the inversion contributes to adaptation and reproductive isolation in natural populations, we conducted a novel reciprocal transplant experiment involving outbred lines, where alternative arrangements of the inversion were reciprocally introgressed into the genetic backgrounds of each ecotype. Our results demonstrate for the first time in nature the contribution of an inversion to adaptation, an annual/perennial life-history shift, and multiple reproductive isolating barriers. These results are consistent with the local adaptation mechanism being responsible for the distribution of the two inversion arrangements across the geographic range of M. guttatus and that locally adaptive inversion effects contribute directly to reproductive isolation. Such a mechanism may be partially responsible for the observation that closely related species often differ by multiple chromosomal rearrangements.
    PLoS Biology 01/2010; 8(9). · 12.69 Impact Factor
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    ABSTRACT: Soil moisture is a key factor affecting plant abundance and distribution, both across and within species. In response to water limitation, plants have evolved numerous morphological, physiological, and phenological adaptations. In both well-watered and water-limited conditions, we identified considerable natural variation in drought-related whole-plant and leaf-level traits among closely related members of the Mimulus guttatus species complex that occupy a diversity of habitats in the field. The self-fertilizing Mimulus nasutus and serpentine-endemic Mimulus nudatus demonstrated the overall greatest tolerance to soil water limitation, exhibiting the smallest reduction in seed set relative to well-watered conditions. This may be due in part to early flowering, faster fruit development, and low stomatal density. In contrast, flowering of coastal M. guttatus was so delayed that it precluded any seed production in water-limited conditions. This range of phenotypic responses to soil water deficit in Mimulus, coupled with developing genomic resources, holds considerable promise for identifying genomic variation responsible for adaptive responses to soil water availability.
    Oecologia 10/2009; 162(1):23-33. · 3.01 Impact Factor

Publication Stats

433 Citations
124.30 Total Impact Points

Institutions

  • 2012–2014
    • University of Texas at Austin
      • Institute for Cellular and Molecular Biology
      Austin, Texas, United States
  • 2013
    • Harvard University
      Cambridge, Massachusetts, United States
  • 2008–2012
    • Duke University Medical Center
      Durham, North Carolina, United States
  • 2009–2010
    • Duke University
      • Department of Biology
      Durham, North Carolina, United States