Publications

2011
Mueller UG, Mikheyev AS, Hong E, Sen R, Warren DL, Solomon SE, Ishak HD, Cooper M, Miller JL, Shaffer KA, et al. Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant-fungus symbiosis. Proc Natl Acad Sci U S A. 2011;108 (10) :4053-6.Abstract
The obligate mutualism between leafcutter ants and their Attamyces fungi originated 8 to 12 million years ago in the tropics, but extends today also into temperate regions in South and North America. The northernmost leafcutter ant Atta texana sustains fungiculture during winter temperatures that would harm the cold-sensitive Attamyces cultivars of tropical leafcutter ants. Cold-tolerance of Attamyces cultivars increases with winter harshness along a south-to-north temperature gradient across the range of A. texana, indicating selection for cold-tolerant Attamyces variants along the temperature cline. Ecological niche modeling corroborates winter temperature as a key range-limiting factor impeding northward expansion of A. texana. The northernmost A. texana populations are able to sustain fungiculture throughout winter because of their cold-adapted fungi and because of seasonal, vertical garden relocation (maintaining gardens deep in the ground in winter to protect them from extreme cold, then moving gardens to warmer, shallow depths in spring). Although the origin of leafcutter fungiculture was an evolutionary breakthrough that revolutionized the food niche of tropical fungus-growing ants, the original adaptations of this host-microbe symbiosis to tropical temperatures and the dependence on cold-sensitive fungal symbionts eventually constrained expansion into temperate habitats. Evolution of cold-tolerant fungi within the symbiosis relaxed constraints on winter fungiculture at the northern frontier of the leafcutter ant distribution, thereby expanding the ecological niche of an obligate host-microbe symbiosis.
Pantel JH, Leibold MA, Juenger TE. Population differentiation in Daphnia alters community assembly in experimental ponds. Am Nat. 2011;177 (3) :314-22.Abstract
Most studies of community assembly ignore how genetic differentiation within species affects their colonization and extinction. However, genetic differentiation in ecologically relevant traits may be substantial enough to alter the colonization and extinction processes that drive community assembly. We measured significant molecular genetic and quantitative trait differentiation among three Daphnia pulex × pulicaria populations in southwestern Michigan ponds and investigated whether this differentiation could alter the assembly of pond zooplankton communities in experimental mesocosms. In this study, we monitored the invasion success of different D. pulex × pulicaria populations after their introduction into an established zooplankton community. We also monitored the invasion success of a diverse array of zooplankton species into different D. pulex × pulicaria populations. Zooplankton community composition depended on the D. pulex × pulicaria source population. Daphnia pulex × pulicaria from one population failed to invade zooplankton communities, while those from other populations successfully invaded similar communities. If population differentiation in other species plays a role in community assembly similar to that demonstrated in our study, assembly may be more sensitive to evolutionary processes than has been previously generally considered.
Kunte K, Shea C, Aardema ML, Scriber MJ, Juenger TE, Gilbert LE, Kronforst MR. Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies. PLoS Genet. 2011;7 (9) :e1002274.Abstract
Hybrid speciation, or the formation of a daughter species due to interbreeding between two parental species, is a potentially important means of diversification, because it generates new forms from existing variation. However, factors responsible for the origin and maintenance of hybrid species are largely unknown. Here we show that the North American butterfly Papilio appalachiensis is a hybrid species, with genomic admixture from Papilio glaucus and Papilio canadensis. Papilio appalachiensis has a mosaic phenotype, which is hypothesized to be the result of combining sex-linked traits from P. glaucus and P. canadensis. We show that P. appalachiensis' Z-linked genes associated with a cooler thermal habitat were inherited from P. canadensis, whereas its W-linked mimicry and mitochondrial DNA were inherited from P. glaucus. Furthermore, genome-wide AFLP markers showed nearly equal contributions from each parental species in the origin of P. appalachiensis, indicating that it formed from a burst of hybridization between the parental species, with little subsequent backcrossing. However, analyses of genetic differentiation, clustering, and polymorphism based on molecular data also showed that P. appalachiensis is genetically distinct from both parental species. Population genetic simulations revealed P. appalachiensis to be much younger than the parental species, with unidirectional gene flow from P. glaucus and P. canadensis into P. appalachiensis. Finally, phylogenetic analyses, combined with ancestral state reconstruction, showed that the two traits that define P. appalachiensis' mosaic phenotype, obligatory pupal diapause and mimicry, evolved uniquely in P. canadensis and P. glaucus, respectively, and were then recombined through hybridization to form P. appalachiensis. These results suggest that natural selection and sex-linked traits may have played an important role in the origin and maintenance of P. appalachiensis as a hybrid species. In particular, ecological barriers associated with a steep thermal cline appear to maintain the distinct, mosaic genome of P. appalachiensis despite contact and occasional hybridization with both parental species.
2010
Juenger TE, Sen S, Bray E, Stahl E, Wayne T, McKay J, Richards JH. Exploring genetic and expression differences between physiologically extreme ecotypes: comparative genomic hybridization and gene expression studies of Kas-1 and Tsu-1 accessions of Arabidopsis thaliana. Plant Cell Environ. 2010;33 (8) :1268-84.Abstract
Recent studies have documented remarkable genetic variation among Arabidopsis thaliana accessions collected from diverse habitats. Of particular interest are accessions with putatively locally adapted phenotypes - that is, accessions with attributes that are likely adaptive at their sites of origin. These genotypes may provide insight into the genetic basis of adaptive evolution as well as allow the discovery of genes of ecological importance. We studied the physiology, genome content and gene expression of two physiologically extreme accessions (Tsu-1 from Tsushima, Japan and Kas-1 from Kashmir, India). Our study was conducted under two levels of soil moisture and accompanied by physiological measurements to characterize early responses to soil drying. Genomic hybridizations identified 42,503 single feature polymorphisms (SFP) between accessions, providing an initial screen for genetic differences. Transcript profiling identified a large number (5996) of genes exhibiting constitutive differences in expression including genes involved in many biological pathways. Mild soil drying resulted in only subtle physiological responses but resulted in gene expression changes in hundreds of transcripts, including 352 genes exhibiting differential responses between accessions. Our results highlight the value of genomic studies of natural accessions as well as identify a number of candidate genes underlying physiological differences between Tsu-1 and Kas-1.
Des Marais DL, Juenger TE. Pleiotropy, plasticity, and the evolution of plant abiotic stress tolerance. Ann N Y Acad Sci. 2010;1206 :56-79.Abstract
Progress in understanding the mechanisms of adaptive plant abiotic stress response has historically come from two separate fields. Molecular biologists employ mutagenic screens, experimental manipulations, and controlled stress treatment to identify genes that, when perturbed, have fairly large effects on phenotype. By contrast, quantitative and evolutionary geneticists generally study naturally occurring variants to inform multigenic models of trait architecture in an effort to predict, for example, the evolutionary response to selection. We discuss five emerging themes from the molecular study of osmotic stress response: the multigenic nature of adaptive response, the modular organization of response to specific cues, the pleiotropic effects of key signaling proteins, the integration of many environmental signals, and the abundant cross-talk between signaling pathways. We argue that these concepts can be incorporated into existing models of trait evolution and provide examples of what may constitute the molecular basis of plasticity and evolvability of abiotic stress response. We conclude by considering future directions in the study of the functional molecular evolution of abiotic stress response that may facilitate new discoveries in molecular biology, evolutionary studies, and plant breeding.
Santuari L, Pradervand S, Amiguet-Vercher A-M, Thomas J, Dorcey E, Harshman K, Xenarios I, Juenger TE, Hardtke CS. Substantial deletion overlap among divergent Arabidopsis genomes revealed by intersection of short reads and tiling arrays. Genome Biol. 2010;11 (1) :R4.Abstract
Identification of small polymorphisms from next generation sequencing short read data is relatively easy, but detection of larger deletions is less straightforward. Here, we analyzed four divergent Arabidopsis accessions and found that intersection of absent short read coverage with weak tiling array hybridization signal reliably flags deletions. Interestingly, individual deletions were frequently observed in two or more of the accessions examined, suggesting that variation in gene content partly reflects a common history of deletion events.
2009
Walker DM, Juenger TE, Gore AC. Developmental profiles of neuroendocrine gene expression in the preoptic area of male rats. Endocrinology. 2009;150 (5) :2308-16.Abstract
Reproductive function is controlled by GnRH cells and their steroid-sensitive regulatory inputs. The proper maturation of this system is critical to sexual development and maintenance of adult function. However, the molecular mechanisms underlying these developmental changes, and the potential roles of gonadal hormones in sculpting these processes, have not been fully explored. We performed a developmental profile from postnatal day (P) 1 through P60 of a network of five genes in the preoptic area (POA) that are critical to reproduction in male Sprague Dawley rats. GnRH, estrogen receptors-alpha, and -beta, androgen receptor (AR), and progesterone receptor (PR) mRNAs in the POA were assayed, and serum hormones were measured, in developing male rats. We also used a Taqman low-density array to identify candidate genes that may be important in development. Of the five targeted genes, only AR and PR changed robustly (7- and 3- to 4-fold increases, respectively) during development. All of the gonadal serum hormones changed markedly and with very different patterns from their receptor mRNAs: testosterone decreased from P1 to P30 and then increased to P60; progesterone peaked on P30; and estradiol decreased from P1 to P30. Using the Taqman low-density array, we identified several genes that changed dramatically in the POA with development, particularly G protein-coupled receptor 30, IGF-I, vitamin D receptor, estrogen-related receptor-alpha, and thyroid receptor-alpha. Our data demonstrate developmental stage-specific changes in neuroendocrine genes, particularly AR and PR. Moreover, the relationships between hormones and their corresponding receptors undergo dynamic changes across development in male rats.
2008
Steinberg RM, Walker DM, Juenger TE, Woller MJ, Gore AC. Effects of perinatal polychlorinated biphenyls on adult female rat reproduction: development, reproductive physiology, and second generational effects. Biol Reprod. 2008;78 (6) :1091-101.Abstract
Perinatal exposures to endocrine-disrupting chemicals, such as polychlorinated biphenyls (PCBs), can cause latent effects on reproductive function. Here, we tested whether PCBs administered during late pregnancy would compromise reproductive physiology in both the fetally exposed female offspring (F1 generation), as well as in their female offspring (F2 generation). Pregnant Sprague-Dawley rats were treated with the PCB mixture, Aroclor 1221 (A1221; 0, 0.1, 1, or 10 mg/kg), on Embryonic Days 16 and 18. Somatic and reproductive development of F1 and their F2 female offspring were monitored, including ages of eye opening, pubertal landmarks, and serum reproductive hormones. The results showed that low doses of A1221 given during this critical period of neuroendocrine development caused differential effects of A1221 on F1 and F2 female rats. In both generations, litter sex ratio was skewed toward females. In the F1 generation, additional effects were found, including a significant alteration of serum LH in the 1 mg/kg A1221 group. The F2 generation showed more profound alterations, particularly with respect to fluctuations in hormones and reproductive tract tissues across the estrous cycle. On proestrus, the day of the preovulatory GnRH/gonadotropin surge, F2 females whose mothers had been exposed perinatally to A1221 exhibited substantially suppressed LH and progesterone concentrations, and correspondingly smaller uterine and ovarian weights on estrus, compared with F2 descendants of control rats. These latter changes suggest a dysregulation of reproductive physiology. Thus, low levels of exposure to PCBs during late fetal development cause significant effects on the maturation and physiology of two generations of female offspring. These findings have implications for reproductive health and fertility of wildlife and humans.
Kaczorowski RL, Juenger TE, Holtsford TP. Heritability and correlation structure of nectar and floral morphology traits in Nicotiana alata. Evolution. 2008;62 (7) :1738-50.Abstract
The heritability and genetic basis of nectar traits have been rarely studied in the field, where plants are exposed to environmental factors that could mask underlying genetic effects. Heritabilities and variance components were estimated for nectar and morphological traits of Nicotiana alata, using a partial diallel design. The main experiment was conducted in a Missouri experimental garden using a randomized block design with three plant density treatments, whereas a smaller experiment was conducted near native Brazil habitat to compare the environmental variance in traits between Missouri and Brazil. Significant heritability was detected for nectar volume and energy content, and for corolla tube length. Phenotypic correlations were significant between all traits investigated, whereas significant genetic correlations were only found between nectar volume and energy and between corolla limb width and mouth diameter. There were no significant family-by-density interactions detected in the Missouri field environment. All traits differed significantly between Missouri and Brazil environments, but significant genetic by environment (G x E) interactions between Missouri and Brazil were detected for only one trait. This study shows that nectar traits can be heritable despite considerable environmental variation.
Stearns F, Boles S, Hurston H, Vo T, Butler D, Shuham W, Juenger TE. PERMANENT GENETIC RESOURCES: Identification of nuclear microsatellite loci for Ipomopsis aggregata and the distribution of pairwise relatedness in a natural population. Mol Ecol Resour. 2008;8 (2) :437-9.Abstract
Nine microsatellite loci were developed from enriched libraries of scarlet gilia (Ipomopsis aggregata). A screen of 160 individuals from a population identified reduced levels of heterozygosity, low levels of relatedness, and weak spatial genetic patterns. The population inbreeding coefficient was calculated to be 0.19 (SE = 0.04). These patterns are consistent with those expected from low levels of biparental inbreeding in an obligate outcrosser and extensive seed and pollen dispersal. These preliminary data confirm the usefulness of microsatellite markers for breeding system studies of I. aggregata.
Christman MA, Richards JH, McKay JK, Stahl EA, Juenger TE, Donovan LA. Genetic variation in Arabidopsis thaliana for night-time leaf conductance. Plant Cell Environ. 2008;31 (8) :1170-8.Abstract
Night-time leaf conductance (g(night)) and transpiration may have several adaptive benefits related to plant water, nutrient and carbon relations. Little is known, however, about genetic variation in g(night) and whether this variation correlates with other gas exchange traits related to water use and/or native habitat climate. We investigated g(night) in 12 natural accessions and three near isogenic lines (NILs) of Arabidopsis thaliana. Genetic variation in g(night) was found for the natural accessions, and g(night) was negatively correlated with native habitat atmospheric vapour pressure deficit (VPD(air)), suggesting lower g(night) may be favoured by natural selection in drier habitats. However, there were also significant genetic correlations of g(night) with daytime gas exchange traits expected to affect plant fitness [i.e. daytime leaf conductance, photosynthesis and intrinsic water-use efficiency (WUE(i))], indicating that selection on daytime gas exchange traits may result in indirect selection on g(night). The comparison of three NILs to their parental genotypes identified one quantitative trait locus (QTL) contributing to variation in g(night). Further characterization of genetic variation in g(night) within and among populations and species, and of associations with other traits and native habitats will be needed to understand g(night) as a putatively adaptive trait.
McKay JK, Richards JH, Nemali KS, Sen S, Mitchell-Olds T, Boles S, Stahl EA, Wayne T, Juenger TE. Genetics of drought adaptation in Arabidopsis thaliana II. QTL analysis of a new mapping population, KAS-1 x TSU-1. Evolution. 2008;62 (12) :3014-26.Abstract
Despite compelling evidence that adaptation to local climate is common in plant populations, little is known about the evolutionary genetics of traits that contribute to climatic adaptation. A screen of natural accessions of Arabidopsis thaliana revealed Tsu-1 and Kas-1 to be opposite extremes for water-use efficiency and climate at collection sites for these accessions differs greatly. To provide a tool to understand the genetic basis of this putative adaptation, Kas-1 and Tsu-1 were reciprocally crossed to create a new mapping population. Analysis of F(3) families showed segregating variation in both delta(13)C and transpiration rate, and as expected these traits had a negative genetic correlation (r(g)=- 0.3). 346 RILs, 148 with Kas-1 cytoplasm and 198 with Tsu-1 cytoplasm, were advanced to the F(9) and genotyped using 48 microsatellites and 55 SNPs for a total of 103 markers. This mapping population was used for QTL analysis of delta(13)C using F(9) RIL means. Analysis of this reciprocal cross showed a large effect of cytoplasmic background, as well as two QTL for delta(13)C. The Kas-1 x Tsu-1 mapping population provides a powerful new resource for mapping QTL underlying natural variation and for dissecting the genetic basis of water-use efficiency differences.
2007
Steinberg RM, Juenger TE, Gore AC. The effects of prenatal PCBs on adult female paced mating reproductive behaviors in rats. Horm Behav. 2007;51 (3) :364-72.Abstract
Polychlorinated biphenyls (PCBs) are a family of toxicants that persist in measurable quantities in human and wildlife tissues, despite their ban in production in 1977. Some PCB mixtures can act as endocrine disrupting chemicals (EDCs) by mimicking or antagonizing the actions of hormones in the brain and periphery. When exposure to hormonally active substances such as PCBs occurs during vulnerable developmental periods, particularly prenatally or in early postnatal life, they can disrupt sex-specific patterning of the brain, inducing permanent changes that can later be manifested as improper sexual behaviors. Here, we investigated the effects of prenatal exposure to the PCB mixture Aroclor (A) 1221 on adult female reproductive behaviors in a dose-response model in the Sprague-Dawley rat. Using a paced mating paradigm that permits the female to set the timing of mating and control contact with the male during copulation, we were able to uncover significant differences in female-typical sexual activities in A1221-exposed females. Specifically, A1221 causes significant effects on mating trial pacing, vocalizations, ambulation and the female's likelihood to mate. The results further demonstrate that the intermediate treatment group has the greatest number of disrupted endpoints, suggestive of non-linear dose responses to A1221. These data demonstrate that the behavioral phenotype in adulthood is disrupted by low, ecologically relevant exposures to PCBs, and the results have implications for reproductive success and health in wildlife and women.
2006
Juenger TE, Wayne T, Boles S, Symonds VV, McKay J, Coughlan SJ. Natural genetic variation in whole-genome expression in Arabidopsis thaliana: the impact of physiological QTL introgression. Mol Ecol. 2006;15 (5) :1351-65.Abstract
A long-standing and fundamental question in biology is how genes influence complex phenotypes. Combining near-isogenic line mapping with genome expression profiling offers a unique opportunity for exploring the functional relationship between genotype and phenotype and for generating candidate genes for future study. We used a whole-genome microarray produced with ink-jet technology to measure the relative expression level of over 21,500 genes from an Arabidopsis thaliana near-isogenic line (NIL) and its recurrent parent. The NIL material contained two introgressions (bottom of chromosome II and top of chromosome III) of the Cvi-1 ecotype in a Ler-2 ecotype genome background. Each introgression 'captures' a Cvi allele of a physiological quantitative trait loci (QTL) that our previous studies have shown increases transpiration and reduces water-use efficiency at the whole-plant level. We used a mixed model anova framework for assessing sources of expression variability and for evaluating statistical significance in our array experiment. We discovered 25 differentially expressed genes in the introgression at a false-discovery rate (FDR) cut-off of 0.20 and identified new candidate genes for both QTL regions. Several differentially expressed genes were confirmed with QRT-PCR (quantitative reverse transcription-polymerase chain reaction) assays. In contrast, we found no statistically significant differentially expressed genes outside of the QTL introgressions after controlling for multiple tests. We discuss these results in the context of candidate genes, cloning QTL, and phenotypic evolution.
2005
Juenger TE, Sen S, Stowe KA, Simms EL. Epistasis and genotype-environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana. Genetica. 2005;123 (1-2) :87-105.Abstract
A major goal of evolutionary biology is to understand the genetic architecture of the complex quantitative traits that may lead to adaptations in natural populations. Of particular relevance is the evaluation of the frequency and magnitude of epistasis (gene-gene and gene-environment interaction) as it plays a controversial role in models of adaptation within and among populations. Here, we explore the genetic basis of flowering time in Arabidopsis thaliana using a series of quantitative trait loci (QTL) mapping experiments with two recombinant inbred line (RIL) mapping populations [Columbia (Col) x Landsberg erecta (Ler), Ler x Cape Verde Islands (Cvi)]. We focus on the response of RILs to a series of environmental conditions including drought stress, leaf damage, and apical damage. These data were explicitly evaluated for the presence of epistasis using Bayesian based multiple-QTL genome scans. Overall, we mapped fourteen QTL affecting flowering time. We detected two significant QTL-QTL interactions and several QTL-environment interactions for flowering time in the Ler x Cvi population. QTL-environment interactions were due to environmentally induced changes in the magnitude of QTL effects and their interactions across environments--we did not detect antagonistic pleiotropy. We found no evidence for QTL interactions in the Ler x Col population. We evaluate these results in the context of several other studies of flowering time in Arabidopsis thaliana and adaptive evolution in natural populations.
Symonds VV, Godoy VA, Alconada T, Botto JF, Juenger TE, Casal JJ, Lloyd AM. Mapping quantitative trait loci in multiple populations of Arabidopsis thaliana identifies natural allelic variation for trichome density. Genetics. 2005;169 (3) :1649-58.Abstract
The majority of biological traits are genetically complex. Mapping the quantitative trait loci (QTL) that determine these phenotypes is a powerful means for estimating many parameters of the genetic architecture for a trait and potentially identifying the genes responsible for natural variation. Typically, such experiments are conducted in a single mapping population and, therefore, have only the potential to reveal genomic regions that are polymorphic between the progenitors of the population. What remains unclear is how well the QTL identified in any one mapping experiment characterize the genetics that underlie natural variation in traits. Here we provide QTL mapping data for trichome density from four recombinant inbred mapping populations of Arabidopsis thaliana. By aligning the linkage maps for these four populations onto a common physical map, the results from each experiment were directly compared. Seven of the nine QTL identified are population specific while two were mapped in all four populations. Our results show that many lineage-specific alleles that either increase or decrease trichome density persist in natural populations and that most of this genetic variation is additive. More generally, these findings suggest that the use of multiple populations holds great promise for better understanding the genetic architecture of natural variation.
Hausmann NJ, Juenger TE, Sen S, Stowe KA, Dawson TE, Simms EL. Quantitative trait loci affecting delta13C and response to differential water availibility in Arabidopsis thaliana. Evolution. 2005;59 (1) :81-96.Abstract
Phenotypic plasticity is an important response mechanism of plants to environmental heterogeneity. Here, we explored the genetic basis of plastic responses of Arabidopsis thaliana to water deficit by experimentally mapping quantitative trait loci (QTL) in two recombinant inbred populations (Cvi x Ler and Ler x Col). We detected genetic variation and significant genotype-by-environment interactions for many traits related to water use. We also mapped 26 QTL, including six for carbon isotope composition (delta13C). Negative genetic correlations between fruit length and fruit production as well as between flowering time and branch production were corroborated by QTL colocalization, suggesting these correlations are due to pleiotropy or physical linkage. Water-limited plants were more apically dominant with greater root:shoot ratios and higher delta13C (higher water-use efficiency) when compared to well-watered plants. Many of the QTL effects for these traits interacted significantly with the irrigation treatment, suggesting that the observed phenotypic plasticity is genetically based. We specifically searched for epistatic (QTL-QTL) interactions using a two-dimensional genome scan, which allowed us to detect epistasis regardless of additive genetic effects. We found several significant QTL-QTL interactions including three that exhibited environmental dependence. These results provide preliminary evidence for proposed genetic mechanisms underlying phenotypic plasticity.

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