Incursion Preparedness, Citizen Science and Early Detection of Invasive Insects: The Case of Aleurocanthus spiniferus (Hemiptera, Aleyrodidae) in France.

We describe the process by which the quarantine whitefly, Aleurocanthus spiniferus (Hemiptera, Aleyrodidae), was detected in France. The initial observation was made by a volunteer who reported a picture of an adult in the Inventaire National du Patrimoine Naturel (INPN Espèces), a citizen science resource developed by l'Office Français de la Biodiversité and the French Muséum National d'Histoire Naturelle. The specimen was suspected to be A. spiniferus from this picture by one of the expert entomologists in charge of the Hemiptera group validation. Once the species was identified, it was mounted on a slide and the information was officially passed on to the ministry in charge of agriculture via a communication channel set up in advance for this type of situation. The ministry then triggered the regulatory actions planned in the event of the suspected detection of quarantine organisms. Sampling was quickly carried out and the specimens collected on this occasion were formally identified as belonging to the species A. spiniferus. This led to the formalization of an outbreak in France. This sequence of decisions took just two months from the first observation to the implementation of a management plan. This case presents how incursion preparedness contributes to a rapid response. Furthermore, this case exemplifies how citizen science can contribute to the early detection of invasive species and highlights the importance of informing both the general public and professionals about major environmental issues.

Models of Plant Resistance Deployment.

Owing to their evolutionary potential, plant pathogens are able to rapidly adapt to genetically controlled plant resistance, often resulting in resistance breakdown and major epidemics in agricultural crops. Various deployment strategies have been proposed to improve resistance management. Globally, these rely on careful selection of resistance sources and their combination at various spatiotemporal scales (e.g., via gene pyramiding, crop rotations and mixtures, landscape mosaics). However, testing and optimizing these strategies using controlled experiments at large spatiotemporal scales are logistically challenging. Mathematical models provide an alternative investigative tool, and many have been developed to explore resistance deployment strategies under various contexts. This review analyzes 69 modeling studies in light of specific model structures (e.g., demographic or demogenetic, spatial or not), underlying assumptions (e.g., whether preadapted pathogens are present before resistance deployment), and evaluation criteria (e.g., resistance durability, disease control, cost-effectiveness). It highlights major research findings and discusses challenges for future modeling efforts.

Inferring pathogen dynamics from temporal count data: the emergence of Xylella fastidiosa in France is probably not recent.

Unravelling the ecological structure of emerging plant pathogens persisting in multi-host systems is challenging. In such systems, observations are often heterogeneous with respect to time, space and host species, and may lead to biases of perception. The biased perception of pathogen ecology may be exacerbated by hidden fractions of the whole host population, which may act as infection reservoirs. We designed a mechanistic-statistical approach to help understand the ecology of emerging pathogens by filtering out some biases of perception. This approach, based on SIR (Susceptible-Infected-Removed) models and a Bayesian framework, disentangles epidemiological and observational processes underlying temporal counting data. We applied our approach to French surveillance data on Xylella fastidiosa, a multi-host pathogenic bacterium recently discovered in Corsica, France. A model selection led to two diverging scenarios: one scenario without a hidden compartment and an introduction around 2001, and the other with a hidden compartment and an introduction around 1985. Thus, Xylella fastidiosa was probably introduced into Corsica much earlier than its discovery, and its control could be arduous under the hidden compartment scenario. From a methodological perspective, our approach provides insights into the dynamics of emerging plant pathogens and, in particular, the potential existence of infection reservoirs.

Adaptive diversification in heterogeneous environments.

The role of environmental heterogeneity in the evolution of biological diversity has been studied only for simple types of heterogeneities and dispersals. This article broadens previous results by considering heterogeneities and dispersals that are structured by several environmental factors. It studies the evolution of a metapopulation, living in a network of patches connected by dispersal, under the effects of mutation, selection and migration. First, it is assumed that patches are equally connected and that they carry habitats characterized by several factors exerting selection pressures on several individual traits. Habitat factors may vary in the environment independently or they may be correlated. It is shown that correlations between habitat factors promote adaptive diversification and that this effect may be modified by trait interactions on survival. Then, it is assumed that patches are structured by two crossed factors, called the row and column factors, such that patches are more connected when they occur in the same row or in the same column. Environmental patterns in which each habitat appears in each row the same number of times and appears in each column the same number of times are found to hinder adaptive diversification.

Mutual Exclusion between Fungal Species of the Fusarium Head Blight Complex in a Wheat Spike.

Fusarium head blight (FHB) is one of the most damaging diseases of wheat. FHB is caused by a species complex that includes two genera of Ascomycetes: Microdochium and Fusarium. Fusarium graminearum, Fusarium culmorum, Fusarium poae, and Microdochium nivale are among the most common FHB species in Europe and were chosen for these experiments. Field studies and surveys show that two or more species often coexist within the same field or grain sample. In this study, we investigated the competitiveness of isolates of different species against isolates of F. graminearum at the scale of a single spike. By performing point inoculations of a single floret, we ensured that each species was able to establish independent infections and competed for spike colonization only. The fungal colonization was assessed in each spike by quantitative PCR. After establishing that the spike colonization was mainly downwards, we compared the relative colonization of each species in coinoculations. Classical analysis of variance suggested a competitive interaction but remained partly inconclusive because of a large between-spike variance. Further data exploration revealed a clear exclusion of one of the competing species and the complete absence of coexistence at the spike level.

Interactions between head blight pathogens: consequences for disease development and toxin production in wheat spikes.

Head blight (HB) is one of the most damaging diseases on wheat, inducing significant yield losses and toxin accumulation in grains. Fungal pathogens responsible for HB include the genus Microdochium, with two species, and the toxin producer genus Fusarium, with several species. Field studies and surveys show that two or more species can coexist within a same field and coinfect the same plant or the same spike. In the current study, we investigated how the concomitant presence of F. graminearum and another of the HB complex species influences the spike colonization and the toxin production by the fungi. To study these interactions, 17 well-characterized isolates representing five species were inoculated alone or in pairs on wheat spikes in greenhouse and field experiments. The fungal DNA in the grains was estimated by quantitative PCR and toxin contents (deoxynivalenol and nivalenol) by ultraperformance liquid chromatography-UV detection-tandem mass spectrometry. The responses of the different isolates to the presence of a competitor were variable and isolate specific more than species specific. The development of the most aggressive isolates was either unchanged or a slightly increased, while the development of the less aggressive isolates was reduced. The main outcome of the study was that no trend of increased toxin production was observed in coinoculations compared to single inoculations. On the contrary, the amount of toxin produced was often lower than expected in coinoculations. We thus conclude against the hypothesis that the co-occurrence of several HB-causing species in the same field might aggravate the risk linked to fusarium toxins in wheat production.

Evolution of pathogen specialisation in a host metapopulation: joint effects of host and pathogen dispersal.

Metapopulation processes are important determinants of epidemiological and evolutionary dynamics in host-pathogen systems, and are therefore central to explaining observed patterns of disease or genetic diversity. In particular, the spatial scale of interactions between pathogens and their hosts is of primary importance because migration rates of one species can affect both spatial and temporal heterogeneity of selection on the other. In this study we developed a stochastic and discrete time simulation model to specifically examine the joint effects of host and pathogen dispersal on the evolution of pathogen specialisation in a spatially explicit metapopulation. We consider a plant-pathogen system in which the host metapopulation is composed of two plant genotypes. The pathogen is dispersed by air-borne spores on the host metapopulation. The pathogen population is characterised by a single life-history trait under selection, the infection efficacy. We found that restricted host dispersal can lead to high amount of pathogen diversity and that the extent of pathogen specialisation varied according to the spatial scale of host-pathogen dispersal. We also discuss the role of population asynchrony in determining pathogen evolutionary outcomes.

Quantitative resistance can lead to evolutionary changes in traits not targeted by the resistance QTLs.

This paper addresses the general concern in plant pathology that the introduction of quantitative resistance in the landscape can lead to increased pathogenicity. Hereto, we study the hypothetical case of a quantitative trait loci (QTL) acting on pathogen spore production per unit lesion area. To regain its original fitness, the pathogen can break the QTL, restoring its spore production capacity leading to an increased spore production per lesion. Or alternatively, it can increase its lesion size, also leading to an increased spore production per lesion. A data analysis shows that spore production per lesion (affected by the resistance QTL) and lesion size (not targeted by the QTL) are positively correlated traits, suggesting that a change in magnitude of a trait not targeted by the QTL (lesion size) might indirectly affect the targeted trait (spore production per lesion). Secondly, we model the effect of pathogen adaptation towards increased lesion size and analyse its consequences for spore production per lesion. The model calculations show that when the pathogen is unable to overcome the resistance associated QTL, it may compensate for its reduced fitness by indirect selection for increased pathogenicity on both the resistant and susceptible cultivar, but whereby the QTLs remain effective.

Pathogen population dynamics in agricultural landscapes: the Ddal modelling framework.

Modelling processes that occur at the landscape scale is gaining more and more attention from theoretical ecologists to agricultural managers. Most of the approaches found in the literature lack applicability for managers or, on the opposite, lack a sound theoretical basis. Based on the metapopulation concept, we propose here a modelling approach for landscape epidemiology that takes advantage of theoretical results developed in the metapopulation context while considering realistic landscapes structures. A landscape simulator makes it possible to represent both the field pattern and the spatial distribution of crops. The pathogen population dynamics are then described through a matrix population model both stage- and space-structured. In addition to a classical invasion analysis we present a stochastic simulation experiment and provide a complete framework for performing a sensitivity analysis integrating the landscape as an input factor. We illustrate our approach using an example to evaluate whether the agricultural landscape composition and structure may prevent and mitigate the development of an epidemic. Although designed for a fungal foliar disease, our modelling approach is easily adaptable to other organisms.

Shared influence of pathogen and host genetics on a trade-off between latent period and spore production capacity in the wheat pathogen, Puccinia triticina.

Crop pathogens are notorious for their rapid adaptation to their host. We still know little about the evolution of their life cycles and whether there might be trade-offs between fitness components, limiting the evolutionary potential of these pathogens. In this study, we explored a trade-off between spore production capacity and latent period in Puccinia triticina, a fungal pathogen causing leaf rust on wheat. Using a simple multivariate (manova) technique, we showed that the covariance between the two traits is under shared control of host and pathogen, with contributions from host genotype (57%), pathogen genotype (18.4%) and genotype × genotype interactions (12.5%). We also found variation in sign and strength of genetic correlations for the pathogen, when measured on different host varieties. Our results suggest that these important pathogen life-history traits do not freely respond to directional selection and that precise evolutionary trajectories are contingent on the genetic identity of the interacting host and pathogen.

Dynamics of adaptation in spatially heterogeneous metapopulations.

The selection pressure experienced by organisms often varies across the species range. It is hence crucial to characterise the link between environmental spatial heterogeneity and the adaptive dynamics of species or populations. We address this issue by studying the phenotypic evolution of a spatial metapopulation using an adaptive dynamics approach. The singular strategy is found to be the mean of the optimal phenotypes in each habitat with larger weights for habitats present in large and well connected patches. The presence of spatial clusters of habitats in the metapopulation is found to facilitate specialisation and to increase both the level of adaptation and the evolutionary speed of the population when dispersal is limited. By showing that spatial structures are crucial in determining the specialisation level and the evolutionary speed of a population, our results give insight into the influence of spatial heterogeneity on the niche breadth of species.

Variation and selection of quantitative traits in plant pathogens.

The first section presents the quantitative traits of pathogenicity that are most commonly measured by plant pathologists, how the expression of those traits is influenced by environmental factors, and why the traits must be taken into account for understanding pathogen evolution in agricultural systems. Particular attention is given to the shared genetic control of these traits by the host and the pathogen. Next, the review discusses how quantitative traits account for epidemic development and how they can be related to pathogen fitness. The main constraints that influence the evolution of quantitative traits in pathogen populations are detailed. Finally, possible directions for research on the management of pathogen virulence (as defined by evolutionists) and host quantitative resistance are presented. The review evaluates how the theoretical corpus developed by epidemiologists and evolutionists may apply to plant pathogens in the context of agriculture. The review also analyzes theoretical papers and compares the modeling hypotheses to the biological characteristics of plant pathogens.

The dent stage of maize kernels is the most conducive for fumonisin biosynthesis under field conditions.

The fungal pathogen Fusarium verticillioides infects maize ears and produces fumonisins, known for their adverse effects on human and animal health. Basic questions remain unanswered regarding the kernel stage(s) associated with fumonisin biosynthesis and the kernel components involved in fumonisin regulation during F. verticillioides-maize interaction under field conditions. In this 2-year field study, the time course of F. verticillioides growth and fumonisin accumulation in developing maize kernels, along with the variations in kernel pH and amylopectin content, were monitored using relevant and accurate analytical tools. In all experiments, the most significant increase in fumonisin accumulation or in fumonisin productivity (i.e., fumonisin production per unit of fungus) was shown to occur within a very short period of time, between 22/32 and 42 days after inoculation and corresponding to the dent stage. This stage was also characterized by acidification in the kernel pH and a maximum level of amylopectin content. Our data clearly support published results based on in vitro experiments suggesting that the physiological stages of the maize kernel play a major role in regulating fumonisin production. Here we have validated this result for in planta and field conditions, and we demonstrate that under such conditions the dent stage is the most conducive for fumonisin accumulation.

Influence of cultivated landscape composition on variety resistance: an assessment based on wheat leaf rust epidemics.

In plant pathology, the idea of designing variety management strategies at the scale of cultivated landscapes is gaining more and more attention. This requires the identification of effects that take place at large scales on host and pathogen populations. Here, we show how the landscape varietal composition influences the resistance level (as measured in the field) of the most grown wheat varieties by altering the structure of the pathogen populations. For this purpose, we jointly analysed three large datasets describing the wheat leaf rust pathosystem (Puccinia triticina/Triticum aestivum) at the country scale of France with a Bayesian hierarchical model. We showed that among all compatible pathotypes, some were preferentially associated with a variety, that the pathotype frequencies on a variety were affected by the landscape varietal composition, and that the observed resistance level of a variety was linked to the frequency of the most aggressive pathotypes among all compatible pathotypes. This data exploration establishes a link between the observed resistance level of a variety and landscape composition at the national scale. It illustrates that the quantitative aspects of the host-pathogen relationship have to be considered in addition to the major resistance/virulence factors in landscape epidemiology approaches.

Factors of the Fusarium verticillioides-maize environment modulating fumonisin production.

Fumonisins are mycotoxins mainly produced by two Fusarium species: F. verticillioides and F. proliferatum. These toxins are of great concern due to their widespread contamination in maize and their adverse effects on animal and human health. In the past decade, progress was made in identifying the genes required for fumonisin biosynthesis. Additionally, molecular mechanisms involved in the regulation of fumonisin production have been very recently elucidated. By covering the latest advances concerning the factors modulating fumonisin production, this review aims at presenting an integrated approach of the overall mechanisms involved in the regulation of fumonisin biosynthesis during maize kernel colonization.

Local dispersal of Puccinia triticina and wheat canopy structure.

The development of dynamic models jointly to simulate host growth and disease spread necessitates a precise description of pathogen dispersal in relation to canopy structure. In this study, we measured disease spread from a single infected leaf positioned at different heights in wheat canopies. The resulting lesion distribution was described along crop rows and over three leaf layers. The spore sources, although limited to a single leaf, nearly saturated the host surface accessible to the spores. Most of the lesions were found within 30 to 40 cm of the source. The vertical position of the source influenced the lesion distribution and the steepness of the disease gradients. The leaf layer and the wheat row that contained the spore source were the most infected. Close to the source, a few heavily infected leaves produced steep disease gradients, whereas spore diffusion resulted in shallower gradients along the adjacent rows and on the other leaf layers. Depending on the precision needed, the lesion distribution can be described either at the level of leaf layers or by dispersal gradients for each row and leaf layer.

Aggressiveness components and adaptation to a host cultivar in wheat leaf rust.

Experimental evidence on the capacity of pathogen populations to quantitatively adapt to their hosts and on the life traits that are involved is lacking at this time. In this article, we identified a situation in which a leaf rust pathotype (P1) was found at a high frequency on a widely grown cultivar (Soissons) and we tested the hypothesis that P1 was more aggressive on Soissons than other virulent pathotypes (P2 and P3). Several components of the pathogen life cycle were measured on adult wheat plants in two different experiments under greenhouse conditions: latent period, spore production per lesion and per unit of sporulating tissue, uredinium size, and lesion life span. Regardless of the component, pathotype P1 was repeatedly found to be more aggressive than at least one of the other two pathotypes, with differences of 5 to 51%. Breaking down spore production per lesion into uredinium size and spore production per square millimeter of sporulating tissue showed that the three pathotypes presented different aggressiveness profiles, suggesting different development constraints for the pathogen, either for its growth capacity into host tissues or its ability to exploit the host resources for spore production. Although leaf rust pathotypes present a clonal structure, quantitative differences were found for aggressiveness traits within a pathotype.

Autoinfection in wheat leaf rust epidemics.

Autoinfection (within-host inoculum transmission) allows plant pathogens locally to increase their density on an infected host. Estimating autoinfection is of particular importance in understanding epidemic development in host mixtures. More generally, autoinfection influences the rate of host colonization by the pathogen, as well as pathogen evolution. Despite its importance in epidemiological models, autoinfection has not yet been directly quantified. It was measured here on wheat (Triticum aestivum) leaves infected by a pathogenic fungus (Puccinia triticina). Autoinfection was measured either on inoculated leaves or by assessing the local progeny of spontaneous infections, and was described by a model of the form y = microx(alpha), where alpha accounts for host saturation and micro represents the pathogen multiplication rate resulting from autoinfection. It was shown that autoinfection resulted in typical patterns of disease aggregation at the leaf level and influenced lesion distribution in the crop during the first epidemic stages. The parameter micro was calculated by taking overdispersion of the data and density dependence into account. It was found that a single lesion produced between 50 and 200 offspring by autoinfection, within a pathogen generation. By taking into account environmental variability, it was possible to estimate autoinfection under optimal conditions for epidemic development.

Clonality and host selection in the wheat pathogenic fungus Puccinia triticina.

Clonal reproduction in Puccinia triticina, the cause of wheat leaf rust, has long been hypothesized but has never been demonstrated. Using a population genetics approach and microsatellite markers, we analysed genetic diversity of this fungus at each level of genome organisation. Sampling included isolates from two field populations growing on two cultivars carrying specific resistance genes, completed with isolates representing the main pathotypes identified from a national survey. For the two cultivars, populations differentiated according to the distribution of their genotypes and pathotypes. There was a high proportion of repeated genotypes, combined with a significant linkage disequilibrium and a strong negative value for FIS. These three factors, especially heterozygote excess, strongly support the hypothesis of a high rate of clonal reproduction. Each pathotype matched a unique multilocus genotype, except for a few isolates, which were taken to be mutants of the dominant genotype. We discussed the strong relationship between pathotypes and genotypes as the consequence of clonal reproduction combined with a strong selection exerted by host cultivars.