Invading plants remain undetected in a lag phase while they explore suitable climates.

Successful alien species may experience a period of quiescence, known as the lag phase, before becoming invasive and widespread. The existence of lags introduces severe uncertainty in risk analyses of aliens as the present state of species is a poor predictor of future distributions, invasion success and impact. Predicting a species' ability to invade and pose negative impacts requires a quantitative understanding of the commonality and magnitude of lags, environmental factors and mechanisms likely to terminate lag. Using herbarium and climate data, we analysed over 5,700 time series (species × regions) in 3,505 naturalized plant species from nine regions in temperate and tropical climates to quantify lags and test whether there have been shifts in the species' climatic space during the transition from the lag phase to the expansion phase. Lags were identified in 35% of the assessed invasion events. We detected phylogenetic signals for lag phases in temperate climate regions and that annual self-fertilizing species were less likely to experience lags. Where lags existed, they had an average length of 40 years and a maximum of 320 years. Lengthy lags (>100 years) were more likely to occur in perennial plants and less frequent in self-pollinating species. For 98% of the species with a lag phase, the climate spaces sampled during the lag period differed from those in the expansion phase based on the assessment of centroid shifts or degree of climate space overlap. Our results highlight the importance of functional traits for the onset of the expansion phase and suggest that climate discovery may play a role in terminating the lag phase. However, other possibilities, such as sampling issues and climate niche shifts, cannot be ruled out.

Comparative floral development in male and female plants of Palmer amaranth (Amaranthus palmeri).

PREMISE: Characterizing the developmental processes in the transition from hermaphroditism to unisexuality is crucial for understanding floral evolution. Amaranthus palmeri, one of the most devastating weeds in the United States, is an emerging model system for studying a dioecious breeding system and understanding the biological traits of this invasive weed. The objectives of this study were to characterize phases of flower development in A. palmeri and compare organogenesis of flower development in female and male plants. METHODS: Flower buds from male and female plants were dissected for light microscopy. Segments of male and female inflorescences at different stages of development were cut longitudinally and visualized using scanning electron microscopy. RESULTS: Pistillate flowers have two to three styles, one ovary with one ovule, and five obtuse tepals. Staminate flowers have five stamens with five acute tepals. Floral development was classified into 10 stages. The distinction between the two flower types became apparent at stage four by the formation of stamen primordia in staminate flowers, which developed female and male reproductive organs initially, as contrasted to pistillate flowers, which produced carpel primordia only. In staminate flowers, the putative carpel primordia changed little in size and remained undeveloped. CONCLUSIONS: Timing of inappropriate organ termination varies across the two sexes in A. palmeri. Our study suggests that the evolution of A. palmeri from a cosexual ancestral state to complete dioecy is still in progress since males exhibited transient hermaphroditism and females produced strictly pistillate flowers.

Natural variation in photosynthesis and water use efficiency of locally adapted Persian walnut populations under drought stress and recovery.

Persian walnut is a drought-sensitive species with considerable genetic variation in the photosynthesis and water use efficiency of its populations, which is largely unexplored. Here, we aimed to elucidate changes in the efficiency of photosynthesis and water content using a diverse panel of 60 walnut families which were submitted to a progressive drought for 24 days, followed by two weeks of re-watering. Severe water-withholding reduced leaf relative water content (RWC) by 20%, net photosynthetic rate (Pn) by 50%, stomatal conductance (gs) by 60%, intercellular CO2 concentration (Ci) by 30%, and transpiration rate (Tr) by 50%, but improved water use efficiency (WUE) by 25%. Severe water-withholding also inhibited photosystem II functionality as indicated by reduced quantum yield of intersystem electron transport (φEo) and transfer of electrons per reaction center (ET0/RC), also enhanced accumulation of QA (VJ) resulted in the reduction of the photosynthetic performance (PIABS) and maximal quantum yield of PSII (FV/FM); while elevated quantum yield of energy dissipation (φDo), energy fluxes for absorption (ABS/RC) and dissipated energy flux (DI0/RC) in walnut families. Cluster analysis classified families into three main groups (tolerant, moderately tolerant, and sensitive), with the tolerant group from dry climates exhibiting lesser alterations in assessed parameters than the other groups. Multivariate analysis of phenotypic data demonstrated that RWC and biophysical parameters related to the chlorophyll fluorescence such as FV/FM, φEo, φDo, PIABS, ABS/RC, ET0/RC, and DI0/RC represent fast, robust and non-destructive biomarkers for walnut performance under drought stress. Finally, phenotype-environment association analysis showed significant correlation of some photosynthetic traits with geoclimatic factors, suggesting a key role of climate and geography in the adaptation of walnut to its habitat conditions.

Genome-wide association analysis and pathway enrichment provide insights into the genetic basis of photosynthetic responses to drought stress in Persian walnut.

Uncovering the genetic basis of photosynthetic trait variation under drought stress is essential for breeding climate-resilient walnut cultivars. To this end, we examined photosynthetic capacity in a diverse panel of 150 walnut families (1500 seedlings) from various agro-climatic zones in their habitats and grown in a common garden experiment. Photosynthetic traits were measured under well-watered (WW), water-stressed (WS) and recovery (WR) conditions. We performed genome-wide association studies (GWAS) using three genomic datasets: genotyping by sequencing data (∼43 K SNPs) on both mother trees (MGBS) and progeny (PGBS) and the Axiom™ Juglans regia 700 K SNP array data (∼295 K SNPs) on mother trees (MArray). We identified 578 unique genomic regions linked with at least one trait in a specific treatment, 874 predicted genes that fell within 20 kb of a significant or suggestive SNP in at least two of the three GWAS datasets (MArray, MGBS, and PGBS), and 67 genes that fell within 20 kb of a significant SNP in all three GWAS datasets. Functional annotation identified several candidate pathways and genes that play crucial roles in photosynthesis, amino acid and carbohydrate metabolism, and signal transduction. Further network analysis identified 15 hub genes under WW, WS and WR conditions including GAPB, PSAN, CRR1, NTRC, DGD1, CYP38, and PETC which are involved in the photosynthetic responses. These findings shed light on possible strategies for improving walnut productivity under drought stress.

Experimental data manipulations to assess performance of hyperspectral classification models of crop seeds and other objects.

BACKGROUND: Optical sensing solutions are being developed and adopted to classify a wide range of biological objects, including crop seeds. Performance assessment of optical classification models remains both a priority and a challenge. METHODS: As training data, we acquired hyperspectral imaging data from 3646 individual tomato seeds (germination yes/no) from two tomato varieties. We performed three experimental data manipulations: (1) Object assignment error: effect of individual object in the training data being assigned to the wrong class. (2) Spectral repeatability: effect of introducing known ranges (0-10%) of stochastic noise to individual reflectance values. (3) Size of training data set: effect of reducing numbers of observations in training data. Effects of each of these experimental data manipulations were characterized and quantified based on classifications with two functions [linear discriminant analysis (LDA) and support vector machine (SVM)]. RESULTS: For both classification functions, accuracy decreased linearly in response to introduction of object assignment error and to experimental reduction of spectral repeatability. We also demonstrated that experimental reduction of training data by 20% had negligible effect on classification accuracy. LDA and SVM classification algorithms were applied to independent validation seed samples. LDA-based classifications predicted seed germination with RMSE = 10.56 (variety 1) and 26.15 (variety 2), and SVM-based classifications predicted seed germination with RMSE = 10.44 (variety 1) and 12.58 (variety 2). CONCLUSION: We believe this study represents the first, in which optical seed classification included both a thorough performance evaluation of two separate classification functions based on experimental data manipulations, and application of classification models to validation seed samples not included in training data. Proposed experimental data manipulations are discussed in broader contexts and general relevance, and they are suggested as methods for in-depth performance assessments of optical classification models.

Germination niche breadth of invasive Iris pseudacorus (L.) suggests continued recruitment from seeds with global warming.

PREMISE: Understanding recruitment processes of invasive species is central to conservation and management strategies. Iris pseudacorus, an emergent macrophyte, has established invasive populations across a broad global range, and reduces biodiversity in wetland ecosystems. Climate change is altering germination cues, yet studies on the invasion of wetland macrophytes often ignore germination ecology despite its importance to their establishment and spread. METHODS: We explored germination of seeds from invasive I. pseudacorus populations in California in response to seed coat presence or absence, and several environmental factors. Using experimental results in a thermal time model, we derived germination temperature thresholds. RESULTS: Germination of I. pseudacorus seeds did not require cold or warm stratification, and was not affected by seed coat presence or absence. Germination occurred in the dark, although germinability was two- to threefold times greater under light. At constant temperature, thermal time model estimates included 18.3 ± 1.8°C base germination temperature (Tb$({T}_{b}$ ); 28.2 ± 0.5°C optimal temperature (To$({T}_{o}$ ); and 41.0 ± 1.7°C ceiling temperature (Tc$({T}_{c}$ ). Seeds exposed to 36.0°C achieved over 10% germination, and embryos of ungerminated seeds presented 76% viability. Overall, germinability remained relatively low at constant temperatures (≤25%) but was close to 90% under alternating daily temperatures. CONCLUSIONS: Exposure to diurnally fluctuating temperatures is essential for this species to achieve high germination rates. Our study reveals that I. pseudacorus has a broad germination niche supporting its establishment in a relatively wide range of environments, including at high temperatures more frequent with climate change.

Sex dimorphism in dioecious Palmer amaranth (Amaranthus palmeri) in response to water stress.

MAIN CONCLUSION: Phenological isolation can potentially reduce seed output and may be exploited as a novel tool for ecological management of dioecious weeds. Dioecious plants may benefit from a maximized outcrossing and optimal sex-specific resource allocation; however, this breeding system may also be exploited for weed management. Seed production in dioecious species is contingent upon the co-occurrence and co-flowering of the two genders and can be further disturbed by flowering asynchrony. We explored dimorphism in secondary sex characters in Amaranthus palmeri, and tested if reproductive synchrony can be affected by water stress. We have used seeds of A. palmeri from California, Kansas and Texas, and studied secondary sex characters under natural conditions and in response to water stress. Seeds of A. palmeri from California (CA) and Kansas (KS) were cordially provided by Dr. Anil Shrestha (California State University, Fresno, California) and Dr. Dallas E. Peterson (Kansas State University, Manhattan, Kansas), respectively. Seeds of a third population were collected from mature plants (about 30 plants) from a set-aside field in College Station, Texas. A. palmeri showed no sexual dimorphism with regard to the timing of emergence, plant height, and relative growth rate. While the initiation of flowering occurred earlier in males than females, females preceded males in timing of anthesis. Water stress delayed anthesis in males to a greater extent than females increasing the anthesis mismatch between the two sexes by seven days. Our data provide the first evidence of environment-controlled flowering asynchrony in A. palmeri. From a practical point of view, phenological isolation can potentially reduce seed output and may be exploited as a novel tool for ecological management of dioecious weeds.

Perspective: common errors in dose-response analysis and how to avoid them.

Dose-response experiments are conducted to determine the toxicity of chemicals on organisms. The relationship between dose and response is described by different statistical models. The four-parameter log-logistic model is widely used in pesticide sciences to derive biologically relevant parameters such as ED50 and resistance index (RI). However, there are some common errors associated with the calculation of ED50 and RI that can lead to erroneous conclusions. Here we discuss five common errors and propose guidance to avoid them. We suggest (i) all response curves must be fitted simultaneously to allow for proper comparison of parameters across curves, (ii) in the case of nonparallel curves absolute ED50 must be used instead of relative ED50 , (iii) standard errors or confidence intervals of the parameters must be reported, (iv) the e parameter in asymmetrical models is not equal to ED50 and hence absolute ED50 must be estimated, and (v) when the four-parameter log-logistic model returns a negative value for the lower asymptote, which is biologically meaningless in most cases, the model should be reduced to its three-parameter version or other types of model should be applied. The mixed-effects model and the meta-analytic approach are suggested as appropriate to average the parameters across repeated dose-response experiments. © 2021 Society of Chemical Industry.

Asymmetry in fitness-related traits of later-generation hybrids between two invasive species.

PREMISE: The importance of hybridization to invasion has been frequently discussed, with most studies focusing on the comparison of fitness-related traits between F1 hybrids and their parents and the consequences of such fitness differences. However, relatively little attention has been given to late-generation hybrids. Different fitness landscapes could emerge in later generations after hybrids cross with each other or backcross with their parents, which may play an important role in plant invasion and subsequent speciation. METHODS: In this study, artificial crosses were conducted to generate multiple generations, including F1, F2, and backcrosses between two invasive species: Cakile edentula (self-compatible) and C. maritima (self-incompatible). Putative hybrids were also collected in the sympatric zone and compared with their co-occurring parents for phenotypic and genetic differences. RESULTS: Genetic data provided evidence of hybridization happening in the wild, and phenotypic comparisons showed that natural hybrids had intermediate traits between the two species but showed more similarity to C. maritima than to C. edentula. The asymmetry was further identified in artificial generations for several phenotypic characters. Furthermore, backcrosses exhibited different patterns of variation, with backcrosses to C. maritima having higher reproductive output than their counterparts. CONCLUSIONS: Our results suggest that hybridization and introgression (backcrossing) in Cakile species is asymmetric and most likely to favor the proliferation of C. maritima genes in the mixed population and thus help its establishment, a finding that could not be predicted by characterizing F1 hybrids.

Male Linked Genomic Region Determines Sex in Dioecious Amaranthus palmeri.

Dioecy, the separation of reproductive organs on different individuals, has evolved repeatedly in different plant families. Several evolutionary paths to dioecy have been suggested, but the mechanisms behind sex determination is not well understood. The diploid dioecious Amaranthus palmeri represents a well-suited model system to study sex determination in plants. Despite the agricultural importance of the species, the genetic control and evolutionary state of dioecy in A. palmeri is currently unknown. Early cytogenetic experiments did not identify heteromorphic chromosomes. Here, we used whole-genome sequencing of male and female pools from 2 independent populations to elucidate the genetic control of dioecy in A. palmeri. Read alignment to a close monoecious relative and allele frequency comparisons between male and female pools did not reveal significant sex-linked genes. Consequently, we employed an alignment-free k-mer comparison which enabled us to identify a large number of male-specific k-mers. We assembled male-specific contigs comprising a total of almost 2 Mb sequence, proposing a XY sex-determination system in the species. We were able to identify the potential Y chromosome in the A. palmeri draft genome sequence as 90% of our male-specific sequence aligned to a single scaffold. Based on our findings, we suggest an intermediate evolutionary state of dioecy with a young Y chromosome in A. palmeri. Our findings give insight into the evolution of sex chromosomes in plants and may help to develop sustainable strategies for weed management.

Inheritance of breeding system in Cakile (Brassicaceae) following hybridization: implications for plant invasions.

BACKGROUND AND AIMS: Hybridization is commonly assumed to aid invasions through adaptive introgression. In contrast, a recent theoretical model predicted that there can be non-adaptive demographic advantages from hybridization and that the population consequences will depend on the breeding systems of the species and the extent to which subsequent generations are able to interbreed and reproduce. We examined cross-fertilization success and inheritance of breeding systems of two species in order to better assess the plausibility of the theoretical predictions. METHODS: Reciprocal artificial crosses were made to produce F1, F2 and backcrosses between Cakile maritima (self-incompatible, SI) and Cakile edentula (self-compatible, SC) (Brassicaceae). Flowers were emasculated prior to anther dehiscence and pollen was introduced from donor plants to the recipient's stigma. Breeding system, pollen viability, pollen germination, pollen tube growth and reproductive output were then determined. The results were used to replace the assumptions made in the original population model and new simulations were made. KEY RESULTS: The success rate with the SI species as the pollen recipient was lower than when it was the pollen donor, in quantitative agreement with the 'SI × SC rule' of unilateral incompatibility. Similar outcomes were found in subsequent generations where fertile hybrids were produced but lower success rates were observed in crosses of SI pollen donors with SC pollen recipients. Much lower proportions of SC hybrids were produced than expected from a single Mendelian allele. When incorporated into a population model, these results predicted an even faster rate of replacement of the SC species by the SI species than previously reported. CONCLUSIONS: Our study of these two species provides even clearer support for the feasibility of the non-adaptive hybridization hypothesis, whereby the colonization of an SI species can be assisted by transient hybridization with a congener. It also provides novel insight into reproductive biology beyond the F1 generation.

Outstanding Challenges in the Transferability of Ecological Models.

Predictive models are central to many scientific disciplines and vital for informing management in a rapidly changing world. However, limited understanding of the accuracy and precision of models transferred to novel conditions (their 'transferability') undermines confidence in their predictions. Here, 50 experts identified priority knowledge gaps which, if filled, will most improve model transfers. These are summarized into six technical and six fundamental challenges, which underlie the combined need to intensify research on the determinants of ecological predictability, including species traits and data quality, and develop best practices for transferring models. Of high importance is the identification of a widely applicable set of transferability metrics, with appropriate tools to quantify the sources and impacts of prediction uncertainty under novel conditions.

Iran's Land Suitability for Agriculture.

Increasing population has posed insurmountable challenges to agriculture in the provision of future food security, particularly in the Middle East and North Africa (MENA) region where biophysical conditions are not well-suited for agriculture. Iran, as a major agricultural country in the MENA region, has long been in the quest for food self-sufficiency, however, the capability of its land and water resources to realize this goal is largely unknown. Using very high-resolution spatial data sets, we evaluated the capacity of Iran's land for sustainable crop production based on the soil properties, topography, and climate conditions. We classified Iran's land suitability for cropping as (million ha): very good 0.4% (0.6), good 2.2% (3.6), medium 7.9% (12.8), poor 11.4% (18.5), very poor 6.3% (10.2), unsuitable 60.0% (97.4), and excluded areas 11.9% (19.3). In addition to overarching limitations caused by low precipitation, low soil organic carbon, steep slope, and high soil sodium content were the predominant soil and terrain factors limiting the agricultural land suitability in Iran. About 50% of the Iran's existing croplands are located in low-quality lands, representing an unsustainable practice. There is little room for cropland expansion to increase production but redistribution of cropland to more suitable areas may improve sustainability and reduce pressure on water resources, land, and ecosystem in Iran.

How to be a good neighbour: Facilitation and competition between two co-flowering species.

Empirical evidence suggests that co-flowering species can facilitate each other through shared pollinators. However, the extent to which one co-flowering species can relieve pollination limitation of another while simultaneously competing for abiotic resource has rarely been examined. Using a deterministic model we explored the demographic outcome for one ("focal") species of its co-occurrence with a species that shares pollinators and competes for both pollinator visitation and abiotic resources. In this paper we showed how the overall impact can be positive or negative, depending on the balance between enhanced fertilization versus increased competition. Our model could predict the density of co-flowering species that will maximize the pollination rate of the focal species by attracting pollinators. Because that density will also give rise to competitive effects, a lower density of co-flowering species is required for optimizing the trade-off between enhanced fertilization and competition so as to give the maximum possible facilitation of reproduction in the focal species. Results were qualitatively different when we considered attractiveness of the co-flowering species, as opposed to its density, because attractiveness, unlike density, had no effect on competition for abiotic resources. Whereas unattractive neighbours would not bring in pollinators, very attractive neighbours would captivate pollinators, not sharing them with the focal species. Thus optimal benefit to the focal species came at intermediate levels of attractiveness in the co-flowering species. This intermediate level of attractiveness in co-flowering species simultaneously maximized pollination and overall facilitation of reproduction for the focal species. The likelihood of facilitation was predicted to decline with the selfing rate of the focal species, revealing an indirect cost for an inbreeding mating system. Whether a co-flowering species can be facilitative depends on the way pollinators respond to the plant density: only a Type III functional response for visitation rate can result in facilitation. Our model provided both a conceptual framework and precise quantitative measures for determining the impacts of a neighbouring co-flowering species on reproduction.

Hybridization can facilitate species invasions, even without enhancing local adaptation.

The founding population in most new species introductions, or at the leading edge of an ongoing invasion, is likely to be small. Severe Allee effects-reductions in individual fitness at low population density-may then result in a failure of the species to colonize, even if the habitat could support a much larger population. Using a simulation model for plant populations that incorporates demography, mating systems, quantitative genetics, and pollinators, we show that Allee effects can potentially be overcome by transient hybridization with a resident species or an earlier colonizer. This mechanism does not require the invocation of adaptive changes usually attributed to invasions following hybridization. We verify our result in a case study of sequential invasions by two plant species where the outcrosser Cakile maritima has replaced an earlier, inbreeding, colonizer Cakile edentula (Brassicaceae). Observed historical rates of replacement are consistent with model predictions from hybrid-alleviated Allee effects in outcrossers, although other causes cannot be ruled out.