Evolutionary Epidemiology Consequences of Trait-Dependent Control of Heterogeneous Parasites.

AbstractDisease control can induce both demographic and evolutionary responses in host-parasite systems. Foreseeing the outcome of control therefore requires knowledge of the eco-evolutionary feedback between control and system. Previous work has assumed that control strategies have a homogeneous effect on the parasite population. However, this is not true when control targets those traits that confer to the parasite heterogeneous levels of resistance, which can additionally be related to other key parasite traits through evolutionary trade-offs. In this work, we develop a minimal model coupling epidemiological and evolutionary dynamics to explore possible trait-dependent effects of control strategies. In particular, we consider a parasite expressing continuous levels of a trait-determining resource exploitation and a control treatment that can be either positively or negatively correlated with that trait. We demonstrate the potential of trait-dependent control by considering that the decision maker may want to minimize both the damage caused by the disease and the use of treatment, due to possible environmental or economic costs. We identify efficient strategies showing that the optimal type of treatment depends on the amount applied. Our results pave the way for the study of control strategies based on evolutionary constraints, such as collateral sensitivity and resistance costs, which are receiving increasing attention for both public health and agricultural purposes.

Brown Rot Disease in Stored Nectarines: Modeling the Combined Effects of Preharvest and Storage Conditions.

Brown rot in stored stone fruits, caused by Monilinia spp., may be due to preharvest and storage factors, but the combined effect of these factors has yet to be investigated. We set up two experiments to monitor the progression of brown rot during the storage of nectarines subjected to various preharvest and storage conditions. We assessed the effects of different agricultural practices (irrigation regimen × fruit load) and harvest dates on brown rot progress during storage in 2018 and the effect of different storage temperatures in 2019. We found that the cumulative incidence of brown rot during storage increased with individual fruit mass, which was influenced by agricultural practices, and for later harvest dates. It also increased with storage temperature. We observed that during storage no secondary infections developed in nectarines not in direct contact with fruits infected with Monilinia laxa. These findings led to the identification of candidate variables describing the brown rot risk on nectarines during storage, such as individual fruit mass, meteorological conditions before fruit harvest, prevalence of brown rot at harvest, and storage temperature. We used these variables to build a mathematical model for estimating the time-to-appearance of brown rot symptoms in stored nectarines. This model fitted the experimental data well, highlighting the need to pay greater attention to the interaction between preharvest and storage conditions. This model could be used to evaluate management strategies for reducing the impact of brown rot in nectarines during storage.

Modelling interference between vectors of non-persistently transmitted plant viruses to identify effective control strategies.

Aphids are the primary vector of plant viruses. Transient aphids, which probe several plants per day, are considered to be the principal vectors of non-persistently transmitted (NPT) viruses. However, resident aphids, which can complete their life cycle on a single host and are affected by agronomic practices, can transmit NPT viruses as well. Moreover, they can interfere both directly and indirectly with transient aphids, eventually shaping plant disease dynamics. By means of an epidemiological model, originally accounting for ecological principles and agronomic practices, we explore the consequences of fertilization and irrigation, pesticide deployment and roguing of infected plants on the spread of viral diseases in crops. Our results indicate that the spread of NPT viruses can be i) both reduced or increased by fertilization and irrigation, depending on whether the interference is direct or indirect; ii) counter-intuitively increased by pesticide application and iii) reduced by roguing infected plants. We show that a better understanding of vectors' interactions would enhance our understanding of disease transmission, supporting the development of disease management strategies.

A parsimonious mechanistic model of reproductive and vegetative growth in fruit trees predicts consequences of fruit thinning and branch pruning.

Productivity of fruit tree crops depends on the interaction between plant physiology, environmental conditions and agricultural practices. We develop a mechanistic model of fruit tree crops that reliable simulates the dynamics of variables of interest for growers and consequences of agricultural practices while relying on a minimal number of inputs and parameters. The temporal dynamics of carbon content in the different organs (i.e., shoots-S, roots-R and fruits-F) are the result of photosynthesis by S, nutrient supply by R, respiration by S, R and F, competition among different organs, photoperiod and initial system conditions partially controlled by cultural practices. We calibrate model parameters and evaluate model predictions using unpublished data from a peach (Prunus persica) experimental orchard with trees subjected to different levels of branch pruning and fruit thinning. Fiinally, we evaluate the consequences of different combinations of pruning and thinning intensities within a multi-criteria analysis. The predictions are in good agreement with the experimental measurements and for the different conditions (pruning and thinning). Our simulations indicate that thinning and pruning practices actually used by growers provide the best compromise between total shoot production, which impacts next year's abundance of shoots and fruits, and current year's fruit production in terms of quantity (yield) and quality (average fruit size). This suggests that growers are not only interested in maximizing current year's yield but also in its quality and its durability. The present work provides for modelers a system of equations based on acknowledged principles of plant science easily modifiable for different purposes. For horticulturists, it gives insights on the potentialities of pruning and thinning. For ecologists, it provides a transparent quantitative framework that can be coupled with biotic and abiotic stressors.

An ecophysiological model of plant-pest interactions: the role of nutrient and water availability.

Empirical studies have shown that particular irrigation/fertilization regimes can reduce pest populations in agroecosystems. This appears to promise that the ecological concept of bottom-up control can be applied to pest management. However, a conceptual framework is necessary to develop a mechanistic basis for empirical evidence. Here, we couple a mechanistic plant growth model with a pest population model. We demonstrate its utility by applying it to the peach-green aphid system. Aphids are herbivores which feed on the plant phloem, deplete plants' resources and (potentially) transmit viral diseases. The model reproduces system properties observed in field studies and shows under which conditions the diametrically opposed plant vigour and plant stress hypotheses find support. We show that the effect of fertilization/irrigation on the pest population cannot be simply reduced as positive or negative. In fact, the magnitude and direction of any effect depend on the precise level of fertilization/irrigation and on the date of observation. We show that a new synthesis of experimental data can emerge by embedding a mechanistic plant growth model, widely studied in agronomy, in a consumer-resource modelling framework, widely studied in ecology. The future challenge is to use this insight to inform practical decision making by farmers and growers.

Coupling epidemiological and tree growth models to control fungal diseases spread in fruit orchards.

Agronomic practices can alter plant susceptibility to diseases and represent a promising alternative to the use of pesticides. Yet, they also alter crop quality and quantity so that the evaluation of their efficacy is not straightforward. Here we couple a compartmental epidemiological model for brown rot diffusion in fruit orchards with a fruit-tree growth model explicitly considering the role of agronomic practices over fruit quality. The new modelling framework permits us to evaluate, in terms of quantity and quality of the fruit production, management scenarios characterized by different levels of regulated deficit irrigation and crop load. Our results suggest that a moderate water stress in the final weeks of fruit development and a moderate fruit load provide effective control on the brown rot spreading, and eventually guarantee monetary returns similar to those that would be obtained in the absence of the disease.

A Model for Temporal Dynamics of Brown Rot Spreading in Fruit Orchards.

Brown rot, caused by Monilinia spp., is a major disease of stone fruit and, in favorable environmental conditions and in the absence of fungicide treatments, it causes important economic losses. In the present work, we propose a modification of classical susceptible, exposed, infectious and removed compartmental models to grasp the peculiarities of the progression of brown rot epidemics in stone fruit orchards in the last stage of the fruit growth (i.e., from the end of the pit hardening to harvest time). Namely, we took into account (i) the lifespan of airborne spores; (ii) the dependence of the latent period on the cuticle crack surface area, which itself varies in time with fruit growth; (iii) the impossibility of recovery in infectious fruit; and (iv) the abrupt interruption of disease development by the elimination of the host fruit at harvest time. We parametrized the model by using field data from a peach Prunus persica orchard infected by Monilinia laxa and M. fructicola in Avignon (southern France). The basic reproduction number indicates that the environmental conditions met in the field were extremely favorable to disease development and the model closely fitted the temporal evolution of the fruit abundance in the different epidemiological compartments. The model permits us to highlight crucial mechanisms undergoing brown rot build up and to evaluate the consequences of different agricultural practices on the quantity and quality of the yield. We found that winter sanitation practices (which decrease the initial infection incidence) and the control of the fruit load (which affects the host fruit density and the single fruit growth trajectory) can be effective in controlling brown rot in conjunction with or in place of fungicide treatments.

A global viability assessment of the European eel.

The global European eel (Anguilla anguilla) stock is critically endangered according to the IUCN, and the European Commission has urged the development of conservation plans aimed to ensure its viability. However, the complex life cycle of this panmictic species, which reproduces in the open ocean but spends most of its prereproductive life in continental waters (thus embracing a huge geographic range and a variety of habitat types), makes it difficult to assess the long-term effectiveness of conservation measures. The interplay between local and global stressors raises intriguing cross-scale conservation challenges that require a comprehensive modelling approach to be addressed. We developed a full life cycle model of the global European eel stock, encompassing both the oceanic and the continental phases of eel's life, and explicitly allowing for spatial heterogeneity in vital rates, availability of suitable habitat and settlement potential via a metapopulation approach. We calibrated the model against a long-term time series of global European eel catches and used it to hindcast the dynamics of the stock in the past and project it over the 21st century under different management scenarios. Although our analysis relies on a number of inevitable simplifying assumptions and on data that may not embrace the whole range of variation in population dynamics at the small spatiotemporal scale, our hindcast is consistent with the general pattern of decline of the stock over recent decades. The results of our projections suggest that (i) habitat loss played a major role in the European eel decline; (ii) the viability of the global stock is at risk if appropriate protection measures are not implemented; (iii) the recovery of spawner escapement requires that fishing mortality is significantly reduced; and (iv) the recovery of recruitment might not be feasible if reproductive output is not enhanced.

Fishery-induced selection for slow somatic growth in European eel.

Both theoretical and experimental studies have shown that fishing mortality can induce adaptive responses in body growth rates of fishes in the opposite direction of natural selection. We compared body growth rates in European eel (Anguilla anguilla) from three Mediterranean stocks subject to different fishing pressure. Results are consistent with the hypotheses that i) fast-growing individuals are more likely to survive until sexual maturity than slow-growing ones under natural conditions (no fishing) and ii) fishing can select for slow-growing individuals by removing fast-growing ones. Although the possibility of human-induced evolution seems remote for a panmictic species like such as the European eel, further research is desirable to assess the implications of the intensive exploitation on this critically endangered fish.

A simple model to predict the probability of a peach (Prunus persicae) tree bud to develop as a long or short shoot as a consequence of winter pruning intensity and previous year growth.

In many woody plants, shoots emerging from buds can develop as short or long shoots. The probability of a bud to develop as a long or short shoot relies upon genetic, environmental and management factors and controlling it is an important issue in commercial orchard. We use peach (Prunus persicae) trees, subjected to different winter pruning levels and monitored for two years, to develop and calibrate a model linking the probability of a bud to develop as a long shoot to winter pruning intensity and previous year vegetative growth. Eventually we show how our model can be used to adjust pruning intensity to obtain a desired proportion of long and short shoots.

Allometric scaling of mortality rates with body mass in abalones.

The existence of an allometric relationship between mortality rates and body mass has been theorized and extensively documented across taxa. Within species, however, the allometry between mortality rates and body mass has received substantially less attention and the consistency of such scaling patterns at the intra-specific level is controversial. We reviewed 73 experimental studies to examine the relationship between mortality rates and body size among seven species of abalone (Haliotis spp.), a marine herbivorous mollusk. Both in the field and in the laboratory, log-transformed mortality rates were negatively correlated with log-transformed individual body mass for all species considered, with allometric exponents remarkably similar among species. This regular pattern confirms previous findings that juvenile abalones suffer higher mortality rates than adult individuals. Field mortality rates were higher overall than those measured in the laboratory, and the relationship between mortality and body mass tended to be steeper in field than in laboratory conditions for all species considered. These results suggest that in the natural environment, additional mortality factors, especially linked to predation, could significantly contribute to mortality, particularly at small body sizes. On the other hand, the consistent allometry of mortality rates versus body mass in laboratory conditions suggests that other sources of mortality, beside predation, are size-dependent in abalone.

An integrated genetic-demographic model to unravel the origin of genetic structure in European eel (Anguilla anguilla L.).

The evolutionary enlightened management of species with complex life cycles often requires the development of mathematical models integrating demographic and genetic data. The genetic structure of the endangered European eel (Anguilla anguilla L.) has been thoroughly analyzed in several studies in the past years. However, the interpretation of the key demographic and biologic processes that determine the observed spatio-temporal genetic structure has been very challenging owing to the complex life cycle of this catadromous species. Here, we present the first integrated demographic-genetic model applied to the European eel that explicitly accounts for different levels of larval and adult mixing during oceanic migrations and allows us to explore alternative hypotheses on genetic differentiation. Our analyses show that (i) very low levels of mixing occurring during larval dispersal or adult migration are sufficient to erase entirely any genetic differences among sub-populations; (ii) small-scale temporal differentiation in recruitment can arise if the spawning stock is subdivided in distinct reproductive groups; and (iii) the geographic differentiation component might be overestimated if a limited number of temporal recruits are analyzed. Our study can inspire the scientific debate on the interpretation of genetic structure in other species characterized by complex life cycle and long-range migrations.

Genetic patchiness in European eel adults evidenced by molecular genetics and population dynamics modelling.

Disentangling the demographic processes that determine the genetic structure of a given species is a fundamental question in conservation and management. In the present study, the population structure of the European eel was examined with a multidisciplinary approach combining the fields of molecular genetics and population dynamics modelling. First, we analyzed a total of 346 adult specimens of known age collected in three separate sample sites using a large panel of 22 EST-linked microsatellite loci. Second, we developed a European eel-specific model to unravel the demographic mechanisms that can produce the level of genetic differentiation estimated by molecular markers. This is the first study that reveals a pattern of genetic patchiness in maturing adults of the European eel. A highly significant genetic differentiation was observed among samples that did not follow an Isolation-by-Distance or Isolation-by-Time pattern. The observation of genetic patchiness in adults is likely to result from a limited parental contribution to each spawning event as suggested by our modelling approach. The value of genetic differentiation found is predicted by the model when reproduction occurs in a limited number of spawning events isolated from each other in time or space, with an average of 130-375 breeders in each spawning event. Unpredictability in spawning success may have important consequences for the life-history evolution of the European eel, including a bet-hedging strategy (distributing reproductive efforts over time) which could in turn guarantee successful reproduction of some adults.

Intra-specific scaling of natural mortality in fish: the paradigmatic case of the European eel.

Identifying factors and processes influencing natural mortality is fundamental to the understanding of population dynamics. Metabolic theory of ecology and experimental studies at the cross-species level suggest the existence of general patterns linking natural mortality to body mass and temperature. However, there is scant evidence that similar relationships also hold at the intra-specific scale, possibly because of the relatively narrow range of sizes and temperatures experienced by most species and the effect of local adaptation, which can obscure links between temperature and vital rates. In this sense, the European eel Anguilla anguilla, a panmictic species with a wide distribution range, provides a paradigmatic case. We compiled data published in the past 30 years on eel mortality during the continental phase of the life cycle for 15 eel stocks and calibrated a general model for mortality, considering the effects of body mass, temperature, stock density and gender. Estimated activation energy (E = 1.2 eV) was at the upper extreme reported for metabolic reactions. Estimated mortality rates (ranging between 0.02 year(-1) at 8°C, low density and 0.47 year(-1) at 18°C, high density for a body mass of 100 g) were appreciably lower than those of most fishes, most likely due to the exceptionally low energy-consuming metabolism of eel.