Olfaction in the Anthropocene: NO3 negatively affects floral scent and nocturnal pollination.

There is growing concern about sensory pollutants affecting ecological communities. Anthropogenically enhanced oxidants [ozone (O3) and nitrate radicals (NO3)] rapidly degrade floral scents, potentially reducing pollinator attraction to flowers. However, the physiological and behavioral impacts on pollinators and plant fitness are unknown. Using a nocturnal flower-moth system, we found that atmospherically relevant concentrations of NO3 eliminate flower visitation by moths, and the reaction of NO3 with a subset of monoterpenes is what reduces the scent's attractiveness. Global atmospheric models of floral scent oxidation reveal that pollinators in certain urban areas may have a reduced ability to perceive and navigate to flowers. These results illustrate the impact of anthropogenic pollutants on an animal's olfactory ability and indicate that such pollutants may be critical regulators of global pollination.

Plant response to water stress of native and non-native Oenothera drummondii populations.

Invasive plants can spread over climatically diverse areas. We explore the effects of drought on gas exchange and water relations on the invasive dune species Oenothera drummondii, using plants from four populations with different rainfall and temperatures regimes. Plant material was obtained germinating plants from one native and three non-native populations in a greenhouse. Drought stress was induced by withholding water. Responses to drought stressed plants were then compared to well-watered controls. Measurements of gas exchange, chlorophyll fluorescence and leaf traits were taken initially and every 10 days after water was withheld, until day 36 when plants were re-watered and recover capacity was measured. The effect of water stress was more evident in Fv/Fm and gas exchange variables. The results suggest that this species possess a mechanism of thermal dissipation of energy. Leaf relative water content was significant lower in drought stressed than control plants. At the end of withholding water period, stressed plants are separated from control plants along the axis I of the ordination analysis evidencing differences in functional traits. All plants recovered well after re-watering. Our results provide evidence for permanent differences in morphological traits and functional responses to drought stress among native and invasive populations of O. drummondii. Although we have only studied four populations, these results may provide evidence for the role of plasticity in contributing to the invasion success of this species.

Testing for latitudinal gradients in defense at the macroevolutionary scale.

Plant defenses against herbivores are predicted to evolve to be greater in warmer climates, such as lower latitudes where herbivore pressure is also thought to be higher. Instead, recent findings are often inconsistent with this expectation, suggesting alternative hypotheses are needed. We tested for latitudinal gradients in plant defense evolution at the macroevolutionary scale by characterizing plant chemical defenses across 80 species of the evening primroses, spanning both North and South America. We quantified phenolics in leaves, flowers, and fruits, using advanced analytical chemistry techniques. Dominant individual ellagitannin compounds, total concentrations of ellagitannins, flavonoids, total phenolics, and compound diversity were quantified. Variation in these compounds was predicted with latitude, temperature, precipitation, and continent using phylogenetic generalized least squares (PGLS) multiple regression models. Latitude did not strongly explain variation in chemical defenses. Instead, fruit total ellagitannins, oenothein A, and total phenolics were greater in species inhabiting regions with colder climates. Using analytical chemistry and 80 species in two continents, we show that contrary to classic predictions, concentrations of secondary metabolites are not greater at lower latitudes or in warmer regions. We propose higher herbivore pressure in colder climates and gradients in resource availability as potential drivers of the observed patterns in Oenothera.

Land-use change has no detectable effect on reproduction of a disturbance-adapted, hawkmoth-pollinated plant species.

PREMISE OF THE STUDY: Land-use change is cited as a primary driver of global biodiversity loss, with myriad consequences for species, populations, and ecosystems. However, few studies have examined its impact on species interactions, particularly pollination. Furthermore, when the effects of land-use change on pollination have been studied, the focus has largely been on species pollinated by diurnal pollinators, namely, bees and butterflies. Here, we focus on Oenothera harringtonii, a night-flowering, disturbance-adapted species that has experienced a range-wide gradient of land-use change. We tested the hypothesis that the negative impacts of land-use change are mitigated by long-distance pollination. METHODS: Our study included both temporal (4 yr) and spatial (19 populations range-wide, and 1, 2, and 5 km from the population center) data, providing a comprehensive understanding of the role of land-use change on pollination biology and reproduction. KEY RESULTS: We first confirmed that O. harringtonii is self-incompatible and reliant on pollinators for reproduction. We then showed that hawkmoths (primarily Hyles lineata) are highly reliable and effective pollinators in both space and time. Unlike other studies, we did not detect an effect of population size, increased isolation, or a reduction in suitable habitat in areas with evidence of land-use change on pollination (visitation, pollen removal and deposition). Furthermore, the proportion of suitable habitat and other fragmentation metrics examined were not associated with population size or density in this plant species. CONCLUSIONS: We conclude that nocturnal pollination of Oenothera harringtonii via hawkmoths is robust to the negative impacts of land-use change.

Geographic variation in floral allometry suggests repeated transitions between selfing and outcrossing in a mixed mating plant.

PREMISE OF THE STUDY: Isometric and allometric scaling of a conserved floral plan could provide a parsimonious mechanism for rapid and reversible transitions between breeding systems. This scaling may occur during transitions between predominant autogamy and xenogamy, contributing to the maintenance of a stable mixed mating system. METHODS: We compared nine disjunct populations of the polytypic, mixed mating species Oenothera flava (Onagraceae) to two parapatric relatives, the obligately xenogamous species O. acutissima and the mixed mating species O. triloba. We compared floral morphology of all taxa using principal component analysis (PCA) and developmental trajectories of floral organs using ANCOVA homogeneity of slopes. KEY RESULTS: The PCA revealed both isometric and allometric scaling of a conserved floral plan. Three principal components (PCs) explained 92.5% of the variation in the three species. PC1 predominantly loaded on measures of floral size and accounts for 36% of the variation. PC2 accounted for 35% of the variation, predominantly in traits that influence pollinator handling. PC3 accounted for 22% of the variation, primarily in anther-stigma distance (herkogamy). During O. flava subsp. taraxacoides development, style elongation was accelerated relative to anthers, resulting in positive herkogamy. During O. flava subsp. flava development, style elongation was decelerated, resulting in zero or negative herkogamy. Of the two populations with intermediate morphology, style elongation was accelerated in one population and decelerated in the other. CONCLUSIONS: Isometric and allometric scaling of floral organs in North American Oenothera section Lavauxia drive variation in breeding system. Multiple developmental paths to intermediate phenotypes support the likelihood of multiple mating system transitions.

Recurrent loss of sex is associated with accumulation of deleterious mutations in Oenothera.

Sexual reproduction is nearly universal among eukaryotes. Theory predicts that the rarity of asexual eukaryotic species is in part caused by accumulation of deleterious mutations and heightened extinction risk associated with suppressed recombination and segregation in asexual species. We tested this prediction with a large data set of 62 transcriptomes from 29 species in the plant genus Oenothera, spanning ten independent transitions between sexual and a functionally asexual genetic system called permanent translocation heterozygosity. Illumina short-read sequencing and de novo transcript assembly yielded an average of 16.4 Mb of sequence per individual. Here, we show that functionally asexual species accumulate more deleterious mutations than sexual species using both population genomic and phylogenetic analysis. At an individual level, asexual species exhibited 1.8 × higher heterozygosity than sexual species. Within species, we detected a higher proportion of nonsynonymous polymorphism relative to synonymous variation within asexual compared with sexual species, indicating reduced efficacy of purifying selection. Asexual species also exhibited a greater proportion of transcripts with premature stop codons. The increased proportion of nonsynonymous mutations was also positively correlated with divergence time between sexual and asexual species, consistent with Muller's ratchet. Between species, we detected repeated increases in the ratio of nonsynonymous to synonymous divergence in asexual species compared with sexually reproducing sister taxa, indicating increased accumulation of deleterious mutations. These results confirm that an important advantage of sex is that it facilitates selection against deleterious alleles, which might help to explain the dearth of extant asexual species.

Phytostabilization potential of evening primrose (Oenothera glazioviana) for copper-contaminated sites.

A field investigation, field experiment, and hydroponic experiment were conducted to evaluate feasibility of using Oenothera glazioviana for phytostabilization of copper-contaminated soil. In semiarid mine tailings in Tongling, Anhui, China, O. glazioviana, a copper excluder, was a dominant species in the community, with a low bioaccumulation factor, the lowest copper translocation factor, and the lowest copper content in seed (8 mg kg(-1)). When O. glazioviana was planted in copper-polluted farmland soil in Nanjing, Jiangsu, China, its growth and development improved and the level of γ-linolenic acid in seeds reached 17.1%, compared with 8.73% in mine tailings. A hydroponic study showed that O. glazioviana had high tolerance to copper, low upward transportation capacity of copper, and a high γ-linolenic acid content. Therefore, it has great potential for the phytostabilization of copper-contaminated soils and a high commercial value without risk to human health.

Social dilemmas among supergenes: intragenomic sexual conflict and a selfing solution in Oenothera.

Recombination is a powerful policing mechanism to control intragenomic cheats. The "parliament of the genes" can often rapidly block driving genes from cheating during meiosis. But what if the genome parliament is reduced to only two members, or supergenes? Using a series of simple game-theoretic models inspired by the peculiar genetics of Oenothera sp., we illustrate that a two supergene genome (α and ß) can produce a number of surprising evolutionary dynamics, including increases in lineage longevity following a transition from sexuality (outcrossing) to asexuality (clonal self-fertilization). We end by interpreting the model in the broader context of the evolution of mutualism, which highlights that greater α, ß cooperation in the self-fertilizing model can be viewed as an example of partner fidelity driving multilineage cooperation.

Effects of plant sex on range distributions and allocation to reproduction.

Despite an abundance of theory, few empirical studies have explored the ecological and evolutionary consequences of sex. We used a comparative phylogenetic approach to examine whether transitions between sexual and asexual reproduction are associated with changes in the size and distribution of species' geographical ranges, and their investment in reproduction. Here, we reconstructed the phylogeny of the genus Oenothera sections Oenothera and Calylophus (Onagraceae), which contain 35 sexual and 30 functionally asexual species. From each species, we collected data on the geographical distribution and variation in plant traits related to reproduction. Functionally asexual species occurred at higher latitudes, but did not differ in range size, compared with sexual species. Transitions to asexuality were associated with decreased investment in floral structures, including the length of petals, floral tubes and styles. Decreased anther size and increased seed size within asexual species also suggest altered allocation to male and female fitness. The observed range shifts are consistent with superior colonization of environments by asexual species following glaciation, and the observed changes in reproductive allocation support predictions made by models relating to the evolution of selfing. Our results suggest that the evolutionary consequences of asexual reproduction might be less restrictive than previously thought.

Climate, niche evolution, and diversification of the "bird-cage" evening primroses (Oenothera, sections Anogra and Kleinia).

We integrate climatic niche models and dated phylogenies to characterize the evolution of climatic niches in Oenothera sections Anogra and Kleinia (Onagraceae), and from that we make inferences on diversification in relation to climate. The evolution of climatic tolerances in Anogra + Kleinia has been heterogeneous, across phylogenetic groups and across different dimensions of climate. All the extant taxa occur in semiarid to arid conditions (annual precipitation of 10.1-49.1 cm and high temperatures in the warmest month of 28.5 degrees-40.1 degrees C), but there is striking variation among taxa in their climatic tolerances, especially temperature (minimum temperatures in the coldest month of -14.0 degrees to 5.3 degrees C) and summer versus winter precipitation (precipitation in the warmest quarter of 0.6-19.4 cm). Climatic disparity is especially pronounced in two subclades (californica, deltoides) that radiated in the southwestern United States and California, apparently including both divergent and convergent evolution of climatic tolerances. This niche evolution is remarkable, given the probable timescale of the radiation (approximately 1 million years). We suggest that the spatiotemporal climatic heterogeneity of western North America has served as a driver of diversification. Our data are also consistent with Axelrod's hypothesis that the spread of arid conditions in western North America stimulated diversification of arid-adapted lineages.

Evolution of flowering strategies in Oenothera glazioviana: an integral projection model approach.

The timing of reproduction is a key determinant of fitness. Here, we develop parameterized integral projection models of size-related flowering for the monocarpic perennial Oenothera glazioviana and use these to predict the evolutionarily stable strategy (ESS) for flowering. For the most part there is excellent agreement between the model predictions and the results of quantitative field studies. However, the model predicts a much steeper relationship between plant size and the probability of flowering than observed in the field, indicating selection for a 'threshold size' flowering function. Elasticity and sensitivity analysis of population growth rate lambda and net reproductive rate R(0) are used to identify the critical traits that determine fitness and control the ESS for flowering. Using the fitted model we calculate the fitness landscape for invading genotypes and show that this is characterized by a ridge of approximately equal fitness. The implications of these results for the maintenance of genetic variation are discussed.