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1.
Ecotoxicol Environ Saf ; 277: 116382, 2024 Jun 01.
Article En | MEDLINE | ID: mdl-38677067

Excess copper (Cu) imparts negative effects on plant growth and productivity in soil. To develop the ability of O. biennis to govern pollution soil containing excessive Cu, we investigated seed germination, seedling growth, and seed yield. Furthermore, Cu content and the expression levels of Cu transport related genes in different tissues were measured under exogenous high concentration Cu. O. biennis seeds were sensitive to excess Cu, with an observed reduction in the germination rate, primary root length, fresh weight, and number of seeds germinated daily. Consecutive Cu stress did not cause fatal damage to evening primrose, yet it slowed down plant growth slightly by reducing the leaf water, chlorophyll, plant yield, and seed oil contents while increasing the soluble sugar, proline, malondialdehyde, and H2O2 contents. The Cu content in different organs of O. biennis was disrupted by excess Cu. In particular, the Cu content in O. biennis seeds and seed oil increased and subsequently decreased with the increase of exogenous Cu, reaching a peak under 600 mg·kg-1 consecutive Cu. Furthermore, the 4-month 900 mg·kg-1 Cu treatment did not induce the excessive accumulation of Cu in peels, seeds, and seed oil, maintaining the Cu content within the range required by the Chinese National Food Safety Standards. The treatment also resulted in an upregulation of Cu-uptake (ObCOPT5, ObZIP4, and ObYSL2) and vigorous efflux (ObHMA1) of transport genes, of which expression levels were significant positive correlation (p < 0.05) with the Cu content. Among all organs, the stem replaced the root as the organ exhibited the greatest ability to absorb and store Cu, and even the Cu transport genes could still function continuously in stem under excess Cu. This work identified a species that can tolerate high Cu content in soil while maintaining a high yield. Furthermore, the results revealed the enrichment of Cu to occur primarily in the O. biennis stem rather than the seeds and peel under excess Cu.


Copper , Germination , Oenothera biennis , Seeds , Soil Pollutants , Soil Pollutants/toxicity , Copper/toxicity , Seeds/drug effects , Germination/drug effects , Oenothera biennis/drug effects , Oenothera biennis/genetics , Soil/chemistry , Seedlings/drug effects
2.
BMC Ecol Evol ; 23(1): 66, 2023 11 17.
Article En | MEDLINE | ID: mdl-37974080

BACKGROUND: The evening primrose family (Onagraceae) includes 664 species (803 taxa) with a center of diversity in the Americas, especially western North America. Ongoing research in Onagraceae includes exploring striking variation in floral morphology, scent composition, and breeding system, as well as the role of these traits in driving diversity among plants and their interacting pollinators and herbivores. However, these efforts are limited by the lack of a comprehensive, well-resolved phylogeny. Previous phylogenetic studies based on a few loci strongly support the monophyly of the family and the sister relationship of the two largest tribes but fail to resolve several key relationships. RESULTS: We used a target enrichment approach to reconstruct the phylogeny of Onagraceae using 303 highly conserved, low-copy nuclear loci. We present a phylogeny for Onagraceae with 169 individuals representing 152 taxa sampled across the family, including extensive sampling within the largest tribe, Onagreae. Deep splits within the family are strongly supported, whereas relationships among closely related genera and species are characterized by extensive conflict among individual gene trees. CONCLUSIONS: This phylogenetic resource will augment current research projects focused throughout the family in genomics, ecology, coevolutionary dynamics, biogeography, and the evolution of characters driving diversification in the family.


Oenothera biennis , Onagraceae , Humans , Phylogeny , Oenothera biennis/genetics , Plant Breeding , Genomics
3.
PLoS One ; 17(6): e0269307, 2022.
Article En | MEDLINE | ID: mdl-35749399

The plant genus Oenothera has played an important role in the study of plant evolution of genomes and plant defense and reproduction. Here, we build on the 1kp transcriptomic dataset by creating 44 new transcriptomes and analyzing a total of 63 transcriptomes to present a large-scale comparative study across 29 Oenothera species. Our dataset included 30.4 million reads per individual and 2.3 million transcripts on average. We used this transcriptome resource to examine genome-wide evolutionary patterns and functional diversification by searching for orthologous genes and performed gene family evolution analysis. We found wide heterogeneity in gene family evolution across the genus, with section Oenothera exhibiting the most pronounced evolutionary changes. Overall, more significant gene family expansions occurred than contractions. We also analyzed the molecular evolution of phenolic metabolism by retrieving proteins annotated for phenolic enzymatic complexes. We identified 1,568 phenolic genes arranged into 83 multigene families that varied widely across the genus. All taxa experienced rapid phenolic evolution (fast rate of genomic turnover) involving 33 gene families, which exhibited large expansions, gaining about 2-fold more genes than they lost. Upstream enzymes phenylalanine ammonia-lyase (PAL) and 4-coumaroyl: CoA ligase (4CL) accounted for most of the significant expansions and contractions. Our results suggest that adaptive and neutral evolutionary processes have contributed to Oenothera diversification and rapid gene family evolution.


Oenothera biennis , Oenothera , Onagraceae , Evolution, Molecular , Metabolic Networks and Pathways , Multigene Family , Oenothera/genetics , Oenothera biennis/genetics , Phylogeny , Transcriptome
4.
Proc Natl Acad Sci U S A ; 118(34)2021 08 24.
Article En | MEDLINE | ID: mdl-34400497

Dormancy has repeatedly evolved in plants, animals, and microbes and is hypothesized to facilitate persistence in the face of environmental change. Yet previous experiments have not tracked demography and trait evolution spanning a full successional cycle to ask whether early bouts of natural selection are later reinforced or erased during periods of population dormancy. In addition, it is unclear how well short-term measures of fitness predict long-term genotypic success for species with dormancy. Here, we address these issues using experimental field populations of the plant Oenothera biennis, which evolved over five generations in plots exposed to or protected from insect herbivory. While populations existed above ground, there was rapid evolution of defensive and life-history traits, but populations lost genetic diversity and crashed as succession proceeded. After >5 y of seed dormancy, we triggered germination from the seedbank and genotyped >3,000 colonizers. Resurrected populations showed restored genetic diversity that reduced earlier responses to selection and pushed population phenotypes toward the starting conditions of a decade earlier. Nonetheless, four defense and life-history traits remained differentiated in populations with insect suppression compared with controls. These findings capture key missing elements of evolution during ecological cycles and demonstrate the impact of dormancy on future evolutionary responses to environmental change.


Biological Evolution , Oenothera biennis/genetics , Oenothera biennis/physiology , Plant Dormancy/physiology , Seeds/physiology , Climate Change , Time Factors
5.
Plant Cell ; 33(8): 2583-2601, 2021 08 31.
Article En | MEDLINE | ID: mdl-34048579

Genetic incompatibility between the cytoplasm and the nucleus is thought to be a major factor in species formation, but mechanistic understanding of this process is poor. In evening primroses (Oenothera spp.), a model plant for organelle genetics and population biology, hybrid offspring regularly display chloroplast-nuclear incompatibility. This usually manifests in bleached plants, more rarely in hybrid sterility or embryonic lethality. Hence, most of these incompatibilities affect photosynthetic capability, a trait that is under selection in changing environments. Here we show that light-dependent misregulation of the plastid psbB operon, which encodes core subunits of photosystem II and the cytochrome b6f complex, can lead to hybrid incompatibility, and this ultimately drives speciation. This misregulation causes an impaired light acclimation response in incompatible plants. Moreover, as a result of their different chloroplast genotypes, the parental lines differ in photosynthesis performance upon exposure to different light conditions. Significantly, the incompatible chloroplast genome is naturally found in xeric habitats with high light intensities, whereas the compatible one is limited to mesic habitats. Consequently, our data raise the possibility that the hybridization barrier evolved as a result of adaptation to specific climatic conditions.


Genetic Speciation , Genome, Chloroplast , Oenothera biennis/genetics , Operon , Photosynthesis/genetics , Acclimatization/genetics , Cytochrome b6f Complex/genetics , Light , Oenothera biennis/physiology , Photosystem II Protein Complex/genetics , Plant Proteins/genetics , Plastids/genetics , Promoter Regions, Genetic , RNA Editing
6.
Ecology ; 99(2): 464-473, 2018 02.
Article En | MEDLINE | ID: mdl-29205317

Many clonal organisms occasionally outcross, but the long-term consequences of such infrequent events are often unknown. During five years, representing three to five plant generations, we followed 16 experimental field populations of the forb, Oenothera biennis, originally planted with the same 18 original genotypes. Oenothera biennis usually self fertilizes, which, due to its genetic system (permanent translocation heterozygosity), results in seeds that are clones of the maternal plant. However, rare outcrossing produces genetically novel offspring (but without recombination or increased heterozygosity). We sought to understand whether novel genotypes produced through natural outcrossing had greater fecundity or different multigenerational dynamics compared to our original genotypes. We further assessed whether any differences in fitness or abundances through time between original and novel genotypes were exaggerated in the presence vs. absence of insect herbivores. Over the course of the experiment, we genotyped >12,500 plants using microsatellite DNA markers to identify and track the frequency of specific genotypes and estimated fecundity on a subset (>3,000) of plants. The effective outcrossing rate was 7.3% in the first year and ultimately 50% of the plants were of outcrossed origin by the final year of the experiment. Lifetime fruit production per plant was on average 32% higher across all novel genotypes produced via outcrossing compared to the original genotypes, and this fecundity advantage was significantly enhanced in populations lacking herbivores. Among 43 novel genotypes that were abundant enough to phenotype with replication, plants produced nearly 30% more fruits than the average of their specific two parental genotypes, and marginally more fruits (8%) than their most fecund parent. Mean per capita fecundity of novel genotypes predicted their relative frequencies at the end of the experiment. Novel genotypes increased more dramatically in herbivore-present compared to suppressed populations (45% vs. 27% of all plants), countering the increased competition from dandelions (Taraxacum officinale) that resulted from herbivore suppression. Increased interspecific competition likely also lead to the lower realized fitness of novel vs. original genotypes in herbivore-suppressed populations. These results demonstrate that rare outcrossing and the generation of novel genotypes can create high-fecundity progeny, with the biotic environment influencing the dynamical outcome of such advantages.


Oenothera biennis/genetics , Animals , Genotype , Herbivory , Phenotype , Plants
7.
J Chem Ecol ; 42(8): 772-781, 2016 Aug.
Article En | MEDLINE | ID: mdl-27501815

Plants are hypothesized to evolve increased defense against herbivores at lower latitudes, but an increasing number of studies report evidence that contradicts this hypothesis. Few studies have examined the evolution of constitutive and induced resistance along latitudinal gradients. When induction is not considered, underlying patterns of latitudinal clines in resistance can be obscured because plant resistance represents a combination of induced and constitutive resistance, which may show contrasting patterns with latitude. Here, we asked if there are latitudinal gradients in constitutive versus induced resistance by using genotypes of Oenothera biennis (Onagraceae) sampled along an 18° latitudinal gradient. We conducted two bioassay experiments to compare the resistance of plant genotypes against one generalist (Spodoptera exigua) and one specialist (Acanthoscelidius acephalus) herbivore. These insects were assayed on: i) undamaged control plants, ii) plants that had been induced with jasmonic acid, and iii) plants induced with herbivore damage. Additionally, we examined latitudinal gradients of constitutive and induced chemical resistance by measuring the concentrations of total phenolics, the concentration of oxidized phenolics, and the percentage of phenolics that were oxidized. Spodoptera exigua showed lower performance on plants from lower latitudes, whereas A. acephalus showed no latitudinal pattern. Constitutive total phenolics were greater in plants from lower latitudes, but induced plants showed higher total phenolics at higher latitudes. Oxidative activity was greatest at higher latitudes regardless of induction. Overall, both latitude and induction have an impact on different metrics of plant resistance to herbivory. Further studies should consider the effect of induction and herbivore specialization more explicitly, which may help to resolve the controversy in latitudinal gradients in herbivory and defense.


Geography , Herbivory , Oenothera biennis/physiology , Spodoptera , Weevils , Animals , Evolution, Molecular , Genotype , Oenothera biennis/genetics , Oenothera biennis/metabolism , Phenol/metabolism , Plant Leaves/metabolism
8.
J Evol Biol ; 29(1): 86-97, 2016 01.
Article En | MEDLINE | ID: mdl-26395768

The evolution of plant defence in response to herbivory will depend on the fitness effects of damage, availability of genetic variation and potential ecological and genetic constraints on defence. Here, we examine the potential for evolution of tolerance to deer herbivory in Oenothera biennis while simultaneously considering resistance to natural insect herbivores. We examined (i) the effects of deer damage on fitness, (ii) the presence of genetic variation in tolerance and resistance, (iii) selection on tolerance, (iv) genetic correlations with resistance that could constrain evolution of tolerance and (v) plant traits that might predict defence. In a field experiment, we simulated deer damage occurring early and late in the season, recorded arthropod abundances, flowering phenology and measured growth rate and lifetime reproduction. Our study showed that deer herbivory has a negative effect on fitness, with effects being more pronounced for late-season damage. Selection acted to increase tolerance to deer damage, yet there was low and nonsignificant genetic variation in this trait. In contrast, there was substantial genetic variation in resistance to insect herbivores. Resistance was genetically uncorrelated with tolerance, whereas positive genetic correlations in resistance to insect herbivores suggest there exists diffuse selection on resistance traits. In addition, growth rate and flowering time did not predict variation in tolerance, but flowering phenology was genetically correlated with resistance. Our results suggest that deer damage has the potential to exert selection because browsing reduces plant fitness, but limited standing genetic variation in tolerance is expected to constrain adaptive evolution in O. biennis.


Biological Evolution , Genetic Variation , Herbivory , Oenothera biennis/physiology , Animals , Arthropods , Deer , Insecta , North Carolina , Oenothera biennis/genetics , Phenotype , Plant Leaves/physiology , Selection, Genetic
9.
Ecology ; 96(10): 2632-42, 2015 Oct.
Article En | MEDLINE | ID: mdl-26649385

Plant genetic variation and evolutionary dynamics are predicted to impact ecosystem processes but these effects are poorly understood. Here we test the hypothesis that plant genotype and contemporary evolution influence the flux of energy and nutrients through soil, which then feedback to affect seedling performance in subsequent generations. We conducted a multiyear field evolution experiment using the native biennial plant Oenothera biennis. This experiment was coupled with experimental assays to address our hypothesis and quantify the relative importance of evolutionary and ecological factors on multiple ecosystem processes. Plant genotype, contemporary evolution, spatial variation, and herbivory affected ecosystem processes (e.g., leaf decay, soil respiration, seedling performance, N cycling), but their relative importance varied between specific ecosystem variables. Insect herbivory and evolution also contributed to a feedback that affected seedling biomass of O. biennis in the next generation. Our results show that heritable variation among plant genotypes can be an important factor affecting local ecosystem processes, and while effects of contemporary evolution were detectable and sometimes strong, they were often contingent on other ecological, factors.


Biological Evolution , Ecosystem , Genotype , Oenothera biennis/genetics , Nitrogen/chemistry , Oxygen Consumption , Seedlings/growth & development , Seedlings/metabolism , Soil/chemistry
10.
Ecol Lett ; 18(12): 1376-86, 2015 Dec.
Article En | MEDLINE | ID: mdl-26482702

Greater plant defence is predicted to evolve at lower latitudes in response to increased herbivore pressure. However, recent studies question the generality of this pattern. In this study, we tested for genetically based latitudinal clines in resistance to herbivores and underlying defence traits of Oenothera biennis. We grew plants from 137 populations from across the entire native range of O. biennis. Populations from lower latitudes showed greater resistance to multiple specialist and generalist herbivores. These patterns were associated with an increase in total phenolics at lower latitudes. A significant proportion of the phenolics were driven by the concentrations of two major ellagitannins, which exhibited opposing latitudinal clines. Our analyses suggest that these findings are unlikely to be explained by local adaptation of herbivore populations or genetic variation in phenology. Rather greater herbivory at high latitudes can be explained by latitudinal clines in the evolution of plant defences.


Genetic Variation , Herbivory , Oenothera biennis/physiology , Phenols/metabolism , Biological Evolution , Canada , Oenothera biennis/genetics , Phenotype , United States
11.
Am J Bot ; 101(11): 1906-14, 2014 Nov.
Article En | MEDLINE | ID: mdl-25366856

PREMISE OF THE STUDY: It has long been predicted that a loss of sexual reproduction leads to decreased heritable variation within populations and increased differentiation between populations. Despite an abundance of theory, there are few empirical tests of how sex affects genetic variation in phenotypic traits, especially for plants. Here we test whether repeated losses of two critical components of sex (recombination and segregation) in the evening primroses (Oenothera L., Onagraceae) affect quantitative genetic variation within and between populations. METHODS: We sampled multiple genetic families from 3-5 populations from each of eight Oenothera species, which represented four independent transitions between sexual reproduction and a functionally asexual genetic system called "permanent translocation heterozygosity." We used quantitative genetics methods to partition genetic variation within and between populations for eight plant traits related to growth, leaf physiology, flowering, and resistance to herbivores. KEY RESULTS: Heritability was, on average, 74% higher in sexual Oenothera populations than in functionally asexual populations, with plant growth rate, specific leaf area, and the percentage of leaf water content showing the strongest differences. By contrast, genetic differentiation among populations was 2.8× higher in functionally asexual vs. sexual Oenothera species. This difference was particularly strong for specific leaf area. Sexual populations tended to exhibit higher genetic correlations among traits, but this difference was weakly supported. CONCLUSIONS: These results support the prediction that sexual reproduction maintains higher genetic variation within populations, which may facilitate adaptive evolution. We also found partial support for the prediction that a loss of sex leads to greater population differentiation, which may elevate speciation rates.


Genetic Variation , Oenothera biennis/genetics , Animals , Apomixis , Biological Evolution , Herbivory , Heterozygote , Oenothera biennis/physiology , Parthenogenesis , Phenotype , Reproduction, Asexual
12.
Plant Cell ; 26(3): 1280-93, 2014 Mar.
Article En | MEDLINE | ID: mdl-24681616

Due to reciprocal chromosomal translocations, many species of Oenothera (evening primrose) form permanent multichromosomal meiotic rings. However, regular bivalent pairing is also observed. Chiasmata are restricted to chromosomal ends, which makes homologous recombination virtually undetectable. Genetic diversity is achieved by changing linkage relations of chromosomes in rings and bivalents via hybridization and reciprocal translocations. Although the structural prerequisite for this system is enigmatic, whole-arm translocations are widely assumed to be the mechanistic driving force. We demonstrate that this prerequisite is genome compartmentation into two epigenetically defined chromatin fractions. The first one facultatively condenses in cycling cells into chromocenters negative both for histone H3 dimethylated at lysine 4 and for C-banding, and forms huge condensed middle chromosome regions on prophase chromosomes. Remarkably, it decondenses in differentiating cells. The second fraction is euchromatin confined to distal chromosome segments, positive for histone H3 lysine 4 dimethylation and for histone H3 lysine 27 trimethylation. The end-segments are deprived of canonical telomeres but capped with constitutive heterochromatin. This genomic organization promotes translocation breakpoints between the two chromatin fractions, thus facilitating exchanges of end-segments. We challenge the whole-arm translocation hypothesis by demonstrating why reciprocal translocations of chromosomal end-segments should strongly promote meiotic rings and evolution toward permanent translocation heterozygosity. Reshuffled end-segments, each possessing a major crossover hot spot, can furthermore explain meiotic compatibility between genomes with different translocation histories.


Heterochromatin/genetics , Meiosis , Oenothera biennis/genetics , Translocation, Genetic , Chromosomes, Plant , In Situ Hybridization, Fluorescence , Oenothera biennis/cytology
13.
Isis ; 104(3): 471-503, 2013 Sep.
Article En | MEDLINE | ID: mdl-24341261

Hugo de Vries's mutation theory is now little more than a footnote to the history of biology, a failed theory that briefly led a few biologists astray. However, for the first quarter of the twentieth century it attracted considerable attention from both professional biologists and laypeople. De Vries's theory--together with the plant, Oenothera lamarckiana, that had supplied most of his evidence--became the focus of a surprising variety of imaginative hopes. Scientists and their various publics were fascinated by the utopian possibilities that the primrose seemed to offer, and their discussions shaped a public culture around biology that would help define the twentieth century as the "century of the gene." From a conventional history of science perspective (which, in the case of twentieth-century biology, often remains focused on the content of scientific theories and the professional communities that shaped them), the mutation theory seems unimportant. However, while De Vries's new theory of evolution ultimately failed to persuade the scientific community, it was much more important than is now realized, particularly because it helped make biology part of a wide variety of public debates. Understanding the mutation theory's story more fully suggests that we may need to rethink much of the rest of the century of the gene's history, to think less in terms of what happened in the lab and more about how biology came to function as public culture.


Biological Evolution , Models, Genetic , Mutation , Oenothera biennis/genetics , History, 20th Century , United States
14.
Proc Biol Sci ; 280(1762): 20130639, 2013 Jul 07.
Article En | MEDLINE | ID: mdl-23658201

While plant species diversity can reduce herbivore densities and herbivory, little is known regarding how plant genotypic diversity alters resource utilization by herbivores. Here, we show that an invasive folivore--the Japanese beetle (Popillia japonica)--increases 28 per cent in abundance, but consumes 24 per cent less foliage in genotypic polycultures compared with monocultures of the common evening primrose (Oenothera biennis). We found strong complementarity for reduced herbivore damage among plant genotypes growing in polycultures and a weak dominance effect of particularly resistant genotypes. Sequential feeding by P. japonica on different genotypes from polycultures resulted in reduced consumption compared with feeding on different plants of the same genotype from monocultures. Thus, diet mixing among plant genotypes reduced herbivore consumption efficiency. Despite positive complementarity driving an increase in fruit production in polycultures, we observed a trade-off between complementarity for increased plant productivity and resistance to herbivory, suggesting costs in the complementary use of resources by plant genotypes may manifest across trophic levels. These results elucidate mechanisms for how plant genotypic diversity simultaneously alters resource utilization by both producers and consumers, and show that population genotypic diversity can increase the resistance of a native plant to an invasive herbivore.


Coleoptera/physiology , Genotype , Herbivory , Oenothera biennis/genetics , Animals , New York , Oenothera biennis/growth & development , Population Density
15.
Am Nat ; 181 Suppl 1: S35-45, 2013 May.
Article En | MEDLINE | ID: mdl-23598358

The extent to which evolutionary change occurs in a predictable manner under field conditions and how evolutionary changes feed back to influence ecological dynamics are fundamental, yet unresolved, questions. To address these issues, we established eight replicate populations of native common evening primrose (Oenothera biennis). Each population was planted with 18 genotypes in identical frequency. By tracking genotype frequencies with microsatellite DNA markers over the subsequent three years (up to three generations, ≈5,000 genotyped plants), we show rapid and consistent evolution of two heritable plant life-history traits (shorter life span and later flowering time). This rapid evolution was only partially the result of differential seed production; genotypic variation in seed germination also contributed to the observed evolutionary response. Since evening primrose genotypes exhibited heritable variation for resistance to insect herbivores, which was related to flowering time, we predicted that evolutionary changes in genotype frequencies would feed back to influence populations of a seed predator moth that specializes on O. biennis. By the conclusion of the experiment, variation in the genotypic composition among our eight replicate field populations was highly predictive of moth abundance. These results demonstrate how rapid evolution in field populations of a native plant can influence ecological interactions.


Biological Evolution , Herbivory , Oenothera biennis/genetics , Animals , Ecosystem , Genotype , Moths/physiology , Oenothera biennis/growth & development , Population Density , Seeds/physiology
16.
Science ; 338(6103): 113-6, 2012 Oct 05.
Article En | MEDLINE | ID: mdl-23042894

Insect herbivores are hypothesized to be major factors affecting the ecology and evolution of plants. We tested this prediction by suppressing insects in replicated field populations of a native plant, Oenothera biennis, which reduced seed predation, altered interspecific competitive dynamics, and resulted in rapid evolutionary divergence. Comparative genotyping and phenotyping of nearly 12,000 O. biennis individuals revealed that in plots protected from insects, resistance to herbivores declined through time owing to changes in flowering time and lower defensive ellagitannins in fruits, whereas plant competitive ability increased. This independent real-time evolution of plant resistance and competitive ability in the field resulted from the relaxation of direct selective effects of insects on plant defense and through indirect effects due to reduced herbivory on plant competitors.


Biological Evolution , Ecology , Herbivory/physiology , Moths/physiology , Oenothera biennis/physiology , Animals , Fruit/genetics , Fruit/parasitology , Fruit/physiology , Oenothera biennis/genetics , Oenothera biennis/parasitology , Population , Seeds/genetics , Seeds/parasitology , Seeds/physiology , Selection, Genetic
17.
J Chem Ecol ; 38(8): 992-5, 2012 Aug.
Article En | MEDLINE | ID: mdl-22790783

Root herbivores can affect plant fitness, and roots often contain the same secondary metabolites that act as defenses in shoots, but the ecology and evolution of root chemical defense have been little investigated. Here, we investigated genetic variance, heritability, and correlations among defensive phenolic compounds in shoot vs. root tissues of common evening primrose, Oenothera biennis. Across 20 genotypes, there were roughly similar concentrations of total phenolics in shoots vs. roots, but the allocation of particular phenolics to shoots vs. roots varied along a continuum of genotype growth rate. Slow-growing genotypes allocated 2-fold more of the potential pro-oxidant oenothein B to shoots than roots, whereas fast-growing genotypes had roughly equivalent above and belowground concentrations. Phenolic concentrations in both roots and shoots were strongly heritable, with mostly positive patterns of genetic covariation. Nonetheless, there was genotype-specific variation in the presence/absence of two major ellagitannins (oenothein A and its precursor oenothein B), indicating two different chemotypes based on alterations in this chemical pathway. Overall, the presence of strong genetic variation in root defenses suggests ample scope for the evolution of these compounds as defenses against root herbivores.


Oenothera biennis/chemistry , Evolution, Molecular , Genotype , Hydrolyzable Tannins/metabolism , Oenothera biennis/genetics , Oenothera biennis/growth & development , Plant Roots/chemistry , Plant Shoots/chemistry , Polyphenols/metabolism
18.
J Evol Biol ; 25(8): 1576-86, 2012 Aug.
Article En | MEDLINE | ID: mdl-22587337

Theory predicts that sexual reproduction provides evolutionary advantages over asexual reproduction by reducing mutational load and increasing adaptive potential. Here, we test the latter prediction in the context of plant defences against pathogens because pathogens frequently reduce plant fitness and drive the evolution of plant defences. Specifically, we ask whether sexual evening primrose plant lineages (Onagraceae) have faster rates of adaptive molecular evolution and altered gene expression of a class I chitinase, a gene implicated in defence against pathogens, than functionally asexual evening primrose lineages. We found that the ratio of amino acid to silent substitutions (K(a) /K(s) = 0.19 vs. 0.11 for sexual and asexual lineages, respectively), the number of sites identified to be under positive selection (four vs. zero for sexual and asexual lineages, respectively) and the expression of chitinase were all higher in sexual than in asexual lineages. Our results are congruent with the conclusion that a loss of sexual recombination and segregation in the Onagraceae negatively affects adaptive structural and potentially regulatory evolution of a plant defence protein.


Evolution, Molecular , Oenothera biennis/genetics , Adaptation, Physiological/genetics , Amino Acid Substitution , Chitinases/genetics , Gene Expression Regulation, Plant , Oenothera biennis/classification , Oenothera biennis/enzymology , Reproduction/genetics , Reproduction, Asexual/genetics , Selection, Genetic
19.
Oecologia ; 168(4): 1013-21, 2012 Apr.
Article En | MEDLINE | ID: mdl-22002039

Biodiversity is quantified via richness (e.g., the number of species), evenness (the relative abundance distribution of those species), or proportional diversity (a combination of richness and evenness, such as the Shannon index, H'). While empirical studies show no consistent relationship between these aspects of biodiversity within communities, the mechanisms leading to inconsistent relationships have received little attention. Here, using common evening primrose (Oenothera biennis) and its associated arthropod community, we show that relationships between arthropod richness, evenness, and proportional diversity are altered by plant genotypic richness. Arthropod richness increased with O. biennis genotypic richness due to an abundance-driven accumulation of species in response to greater plant biomass. Arthropod evenness and proportional diversity decreased with plant genotypic richness due to a nonadditive increase in abundance of a dominant arthropod, the generalist florivore/omnivore Plagiognathas politus (Miridae). The greater quantity of flowers and buds produced in polycultures-which resulted from positive complementarity among O. biennis genotypes-increased the abundance of this dominant insect. Using choice bioassays, we show that floral quality did not change in plant genotypic mixtures. These results elucidate mechanisms for how plant genotypic richness can modify relationships between arthropod richness, evenness, and proportional diversity. More broadly, our results suggest that trophic interactions may be a previously underappreciated factor controlling relationships between these different aspects of biodiversity.


Arthropods/physiology , Biodiversity , Food Chain , Genetic Variation , Oenothera biennis/genetics , Analysis of Variance , Animals , Flowers/growth & development , New York , Oenothera biennis/growth & development , Population Density , Population Dynamics
20.
Ecology ; 92(4): 915-23, 2011 Apr.
Article En | MEDLINE | ID: mdl-21661554

Biodiversity loss is proceeding at an unprecedented rate, yet we lack a thorough understanding of the consequences of losing diversity at different scales. While species diversity is known to impact community and ecosystem processes, genotypic diversity is assumed to have relatively smaller effects. Nonetheless, a few recent studies suggest that genotypic diversity may have quantitatively similar ecological consequences compared to species diversity. Here we show that increasing either genotypic diversity of common evening primrose (Oenothera biennis) or species diversity of old-field plant species resulted in nearly equivalent increases (approximately 17%) in aboveground primary production. The predominant mechanism explaining this effect, niche complementarity, was similar for each type of diversity. Arthropod species richness also increased with both types of plant diversity, but the mechanisms leading to this effect differed: abundance-driven accumulation of arthropod species was important in plant genotypic polycultures, whereas resource specialization was important in plant species polycultures. Thus, similar increases in primary productivity differentially impacted higher trophic levels in response to each type of plant diversity. These results highlight important ecological similarities and differences between genotypic and species diversity and suggest that genotypic diversity may play a larger role in community and ecosystem processes than previously realized.


Biodiversity , Genetic Variation , Oenothera biennis/genetics , Plants/genetics , Animals , Arthropods , Models, Biological , Plants/classification
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