Ludovic Mailleret

Epidemiological and evolutionary management of plant resistance: optimizing the deployment of cultivar mixtures in time and space in agricultural landscapes

The management of genes conferring resistance to plant–pathogens should make it possible to control epidemics (epidemiological perspective) and preserve resistance durability (evolutionary perspective). Resistant and susceptible cultivars must be strategically associated according to the principles of cultivar mixture (within a season) and rotation (between seasons). We explored these questions by modeling the evolutionary and epidemiological processes shaping the dynamics of a pathogen population in a landscape composed of a seasonal cultivated compartment and a reservoir compartment hosting pathogen year‐round. Optimal deployment strategies depended mostly on the molecular basis of plant–pathogen interactions and on the agro‐ecological context before resistance deployment, particularly epidemic intensity and landscape connectivity. Mixtures were much more efficient in landscapes in which between‐field infections and infections originating from the reservoir were more prevalent than within‐field infections. Resistance genes requiring two mutations of the pathogen avirulence gene to be broken down, rather than one, were particularly useful when infections from the reservoir predominated. Combining mixture and rotation principles were better than the use of the same mixture each season as (i) they controlled epidemics more effectively in situations in which within‐field infections or infections from the reservoir were frequent and (ii) they fulfilled the epidemiological and evolutionary perspectives.

Allee effects and the evolution of polymorphism in cyclic parthenogens

Cyclic parthenogens alternate asexual reproduction with periodic episodes of sexual reproduction. Sexually produced free-living forms are often their only way to survive unfavorable periods. When sexual reproduction requires the mating of two self-incompatible individuals, mating limitation may generate an Allee effect, which makes small populations particularly vulnerable to extinction; parthenogenetic reproduction can attenuate this effect. However, asexual reproduction likely trades off with sexual reproduction. To explore the evolutionary implications of such a trade-off, we included recurrent mating events associated with seasonal interruptions in a simple population dynamics model. Following an adaptive dynamics approach, we showed that positive density dependence associated with Allee effects in cyclic parthenogens promotes evolutionary divergence in the level of investment in asexual reproduction. Although polymorphism may be transient, morphs mostly investing into sexual reproduction may eventually exclude those predominantly reproducing in an asexual manner. Asexual morphs can be seen as making cooperative investments into the common pool of mates, while sexual morphs defect, survive better, and may eventually fix in the population. Our findings provide a novel hypothesis for the frequent coexistence of sexual and asexual lineages, notably in plant parasitic fungi.

How optimal foragers should respond to habitat changes: a reanalysis of the Marginal Value Theorem

The Marginal Value Theorem (MVT) is a cornerstone of biological theory. It connects the quality and distribution of patches in a fragmented habitat to the optimal time an individual should spend exploiting them, and thus its optimal rate of movement. However, predictions regarding how habitat alterations should impact optimal strategies have remained elusive, with heavy reliance on graphical arguments. Here we derive the sensitivity of realized fitness and optimal residence times to general habitat attributes, for homogeneous and heterogeneous habitats, retaining the level of generality of the MVT. We provide new predictions on how altering travel times, patch qualities and/or relative abundances should affect optimal strategies, and study the consequences of habitat heterogeneity. We show that knowledge of average characteristics is in general not sufficient to predict the change in the average rate of movement. We apply our results to examine the conditions under which the optimal strategies are invariant to scaling. We prove a previously conjectured form of invariance in homogeneous habitats, but show that invariances to scaling are not generic in heterogeneous habitats. We also consider the relative exploitation of patches that differ in quality, clarifying the conditions under which it is adaptive to stay longer on poorer patches.

The Effect of Partial Crop Harvest on Biological Pest Control

In this paper, the effects of periodic partial harvesting of a continuously grown crop on augmentative biological control are analyzed. Partial harvesting can remove a proportion of both pests and biological control agents, so its influence on the control efficiency cannot be a priori neglected. An impulsive model consisting of a general predator-prey model in ODE, augmented by a discrete component to depict releases of biological control agents and the periodic partial harvesting is used. The periods are taken as integer multiples of each other. A stability condition for pest eradication is expressed as the minimal value of the budget per unit time to spend on predators. We consider the partial harvesting period to be fixed by both the plants physiology and market forces so that the only manipulated variable is the release period. It is shown that varying the release period with respect to the harvest period influences the minimal budget value when the former is carried out more often than the latter and has no effect when releases take place as often as or less frequently than the partial harvests.

Time‐lag in extinction dynamics in experimental populations: evidence for a genetic Allee effect?

1. Propagule pressure, i.e. the number of individuals introduced, is thought to be a major predictor of the establishment success of introduced populations in the field. Its influence in laboratory experimental systems has however been questioned. In fact, other factors involved in long-term population persistence, like habitat size, were usually found to explain most of the dynamics of experimental populations. 2. To better understand the respective influence of short- and long-term factors and their potential interaction on extinction dynamics in experimental systems, we investigated the influence of propagule pressure, habitat size and genetic background on the early dynamics of laboratory-based populations of a hymenopteran parasitoid. 3. The amount of demographic variance differed between establishment and persistence phase and was influenced by habitat size and genetic background (geographic strain), but independent of propagule pressure. In contrast, the probability of extinction within five generations depended on the genetic background and on the interaction between propagule pressure and habitat size. Vulnerability to extinction in small size habitats was increased when populations were founded with a small number of individuals, but this effect was delayed until the third to fifth generations. 4. These results indicate that demographic stochasticity is influential during population establishment, but is not affected by the genetic variability of propagules. On the other hand, extinction might be influenced by a genetic Allee effect triggered by the combination of low propagule pressure and genetic drift. Finally, we documented consistent differences between genetic backgrounds in both deterministic and stochastic population dynamics patterns, with major consequences on extinction risk and ultimately population establishment.

Estimating virus effective population size and selection without neutral markers

By combining high-throughput sequencing (HTS) with experimental evolution, we can observe the within-host dynamics of pathogen variants of biomedical or ecological interest. We studied the evolutionary dynamics of five variants of Potato virus Y (PVY) in 15 doubled-haploid lines of pepper. All plants were inoculated with the same mixture of virus variants and variant frequencies were determined by HTS in eight plants of each pepper line at each of six sampling dates. We developed a method for estimating the intensities of selection and genetic drift in a multi-allelic Wright-Fisher model, applicable whether these forces are strong or weak, and in the absence of neutral markers. This method requires variant frequency determination at several time points, in independent hosts. The parameters are the selection coefficients for each PVY variant and four effective population sizes Ne at different time-points of the experiment. Numerical simulations of asexual haploid Wright-Fisher populations subjected to contrasting genetic drift (Ne ∈ [10, 2000]) and selection (|s| ∈ [0, 0.15]) regimes were used to validate the method proposed. The experiment in closely related pepper host genotypes revealed that viruses experienced a considerable diversity of selection and genetic drift regimes. The resulting variant dynamics were accurately described by Wright-Fisher models. The fitness ranks of the variants were almost identical between host genotypes. By contrast, the dynamics of Ne were highly variable, although a bottleneck was often identified during the systemic movement of the virus. We demonstrated that, for a fixed initial PVY population, virus effective population size is a heritable trait in plants. These findings pave the way for the breeding of plant varieties exposing viruses to stronger genetic drift, thereby slowing virus adaptation.

Quantitative trait loci in pepper control the effective population size of two RNA viruses at inoculation

Infection of plants by viruses is a complex process involving several steps: inoculation into plant cells, replication in inoculated cells and plant colonization. The success of the different steps depends, in part, on the viral effective population size (Ne), defined as the number of individuals passing their genes to the next generation. During infection, the virus population will undergo bottlenecks, leading to drastic reductions in Ne and, potentially, to the loss of the fittest variants. Therefore, it is crucial to better understand how plants affect Ne. We aimed to (i) identify the plant genetic factors controlling Ne during inoculation, (ii) understand the mechanisms used by the plant to control Ne and (iii) compare these genetic factors with the genes controlling plant resistance to viruses. Ne was measured in a doubled-haploid population of Capsicum annuum. Plants were inoculated with either a Potato virus Y (PVY) construct expressing the green fluorescent protein or a necrotic variant of Cucumber mosaic virus (CMV). Newas assessed by counting the number of primary infection foci on cotyledons for PVY or the number of necrotic local lesions on leaves for CMV. The number of foci and lesions was correlated (r=0.57) and showed a high heritability (h2=0.93 for PVY and h2=0.98 for CMV). The Ne of the two viruses was controlled by both common quantitative trait loci (QTLs) and virus-specific QTLs, indicating the contribution of general and specific mechanisms. The PVY-specific QTL colocalizes with a QTL that reduces PVY accumulation and the capacity to break down a major-effect resistance gene.

Temporal autocorrelation in host density increases establishment success of parasitoids in an experimental system

Environmental variation is classically expected to affect negatively population growth and to increase extinction risk, and it has been identified as a major determinant of establishment failures in the field. Yet, recent theoretical investigations have shown that the structure of environmental variation and more precisely the presence of positive temporal autocorrelation might alter this prediction. This is particularly likely to affect the establishment dynamics of biological control agents in the field, as host–parasitoid interactions are expected to induce temporal autocorrelation in host abundance. In the case where parasitoid populations display overcompensatory dynamics, the presence of such positive temporal autocorrelation should increase their establishment success in a variable environment. We tested this prediction in laboratory microcosms by introducing parasitoids to hosts whose abundances were manipulated to simulate uncorrelated or positively autocorrelated variations in carrying capacity. We found that environmental variability decreased population size and increased parasitoid population variance, which is classically expected to extinction risk. However, although exposed to significant environmental variation, we found that parasitoid populations experiencing positive temporal autocorrelation in host abundance were more likely to persist than populations exposed to uncorrelated variation. These results confirm that environmental variation is a key determinant of extinction dynamics that can have counterintuitive effects depending on its autocorrelation structure.

Infochemical use and dietary specialization in parasitoids: a meta-analysis

Abstract Many parasitoid species use olfactory cues to locate their hosts. In tritrophic systems, parasitoids of herbivores can exploit the chemical blends emitted by plants in reaction to herbivore‐induced damage, known as herbivore‐induced plant volatiles (HIPVs). In this study, we explored the specificity and innateness of parasitoid responses to HIPVs using a meta‐analysis of data from the literature. Based on the concept of dietary specialization and infochemical use, we hypothesized that (i) specialist parasitoids (i.e., with narrow host ranges) should be attracted to specific HIPV signals, whereas generalist parasitoids (i.e., with broad host ranges) should be attracted to more generic HIPV signals and (ii) specialist parasitoids should innately respond to HIPVs, whereas generalist parasitoids should have to learn to associate HIPVs with host presence. We characterized the responses of 66 parasitoid species based on published studies of parasitoid behavior. Our meta‐analysis showed that (i) as predicted, specialist parasitoids were attracted to more specific signals than were generalist parasitoids but, (ii) contrary to expectations, response innateness depended on a parasitoids target host life stage rather than on its degree of host specialization: parasitoids of larvae were more likely to show an innate response to HIPVs than were parasitoids of adults. This result changes our understanding of dietary specialization and highlights the need for further theoretical research that will help clarify infochemical use by parasitoids.

Optimal resource allocation for biotrophic plant pathogens

A significant class of plant pathogens is constituted by biotrophic fungi. They set up long-term feeding relationships with their hosts. This kind of parasitism decreases competitive abilities of plants in natural environments and reduces yields in agricultural systems. Therefore, it is relevant to develop and validate mathematical models which can help to better understand how related disease associated traits evolve. In this paper, one-season dynamics of a within-host cohort of spore-producing biotrophic fungi is considered. Their within-host multiplication and outer transmission are implemented by the mycelial growth and free-living (spore) forms, respectively. We state and investigate a specific dynamic optimization problem in order to determine how the fungi allocate available host resources between mycelial growth and spore production. The pathogen fitness criterion is introduced as maximization of the reproductive output. The constructed optimal feedback strategy can serve as a benchmark to compare actual infection mechanisms. There is a singular control subregime which plays an important role from the biological point of view. It keeps the average mycelium size equal to a particular steady value and represents an intermediate configuration of the resource allocation. We also analyze the asymptotic behavior of this steady state when the lesion density is large.