Adaptation of Biotrophic Leaf Pathogens to Fertilization-Mediated Changes in Plant Traits: A Comparison of the Optimization Principle to Invasion Fitness.

One of the conclusions of evolutionary ecology applied to agroecosystem management is that sustainable disease management strategies must be adaptive to overcome the immense adaptive potential of crop pathogens. In this context, knowledge of how pathogens adapt to changes in cultural practices is necessary. In this article we address the issue of the evolutionary response of biotrophic crop pathogens to changes in fertilization practices. For this purpose, we compare predictions of latent period evolution based on three empirical fitness measures (seasonal spore production, within-season exponential growth rate, and area under disease progress curves [AUDPCs]) with predictions based on the concept of invasion fitness from adaptive dynamics. We use pairwise invisibility plots to identify the evolutionarily stable strategies (ESSs) of the pathogen latent period. We find that the ESS latent period is in between the latent periods that maximize the seasonal spore production and the within-season exponential growth rate of the pathogen. The latent periods that maximize the AUDPC are similar to those of the ESS latent periods. The AUDPC may therefore be a critical variable to determine the issue of between-strain competition and shape pathogen evolution.

Does the Latent Period of Leaf Fungal Pathogens Reflect Their Trophic Type? A Meta-Analysis of Biotrophs, Hemibiotrophs, and Necrotrophs.

We performed a meta-analysis to search for a relation between the trophic type and latent period of fungal pathogens. The pathogen incubation period and the level of resistance of the hosts were also investigated. This ecological knowledge would help us to more efficiently regulate crop epidemics for different types of pathogens. We gathered latent period data from 103 studies dealing with 51 fungal pathogens of the three major trophic types (25 biotrophs, 15 hemibiotrophs, and 11 necrotrophs), representing 2,542 mean latent periods. We show that these three trophic types display significantly different latent periods. Necrotrophs exhibited the shortest latent periods (<100 degree-days [DD]), biotrophs had intermediate ones (between 100 and 200 DD), and hemibiotrophs had the longest latent periods (>200 DD). We argue that this relation between trophic type and latent period points to two opposing host exploitation strategies: necrotrophs mount a rapid destructive attack on the host tissue, whereas biotrophs and hemibiotrophs avoid or delay the damaging phase. We query the definition of hemibiotrophic pathogens and discuss whether the length of the latent period is determined by the physiological limits inherent to each trophic type or by the adaptation of pathogens of different trophic types to the contrasting conditions experienced in their interaction with the host.

Modelling interaction dynamics between two foliar pathogens in wheat: a multi-scale approach.

Background and Aims: Disease models can improve our understanding of dynamic interactions in pathosystems and thus support the design of innovative and sustainable strategies of crop protections. However, most epidemiological models focus on a single type of pathogen, ignoring the interactions between different parasites competing on the same host and how they are impacted by properties of the canopy. This study presents a new model of a disease complex coupling two wheat fungal diseases, caused by Zymoseptoria tritici (septoria) and Puccinia triticina (brown rust), respectively, combined with a functional-structural plant model of wheat. Methods: At the leaf scale, our model is a combination of two sub-models of the infection cycles for the two fungal pathogens with a sub-model of competition between lesions. We assume that the leaf area is the resource available for both fungi. Due to the necrotic period of septoria, it has a competitive advantage on biotrophic lesions of rust. Assumptions on lesion competition are first tested developing a geometrically explicit model on a simplified rectangular shape, representing a leaf on which lesions grow and interact according to a set of rules derived from the literature. Then a descriptive statistical model at the leaf scale was designed by upscaling the previous mechanistic model, and both models were compared. Finally, the simplified statistical model has been used in a 3-D epidemiological canopy growth model to simulate the diseases dynamics and the interactions at the canopy scale. Key Results: At the leaf scale, the statistical model was a satisfactory metamodel of the complex geometrical model. At the canopy scale, the disease dynamics for each fungus alone and together were explored in different weather scenarios. Rust and septoria epidemics showed different behaviours. Simulated epidemics of brown rust were greatly affected by the presence of septoria for almost all the tested scenarios, but the reverse was not the case. However, shortening the rust latent period or advancing the rust inoculum shifted the competition more in favour of rust, and epidemics became more balanced. Conclusions: This study is a first step towards the integration of several diseases within virtual plant models and should prompt new research to understand the interactions between canopy properties and competing pathogens.

The Implications of Eco-Evolutionary Processes for the Emergence of Marine Plankton Community Biogeography.

Models of community assembly have been used to illustrate how the many functionally diverse species that compose plankton food webs can coexist. However, the evolutionary processes leading to the emergence of plankton food webs and their interplay with migratory processes and spatial heterogeneity are yet to be explored. We study the eco-evolutionary dynamics of a modeled plankton community structured in both size and space and physiologically constrained by empirical data. We demonstrate that a complex yet ecologically and evolutionarily stable size-structured food web can emerge from an initial set of two monomorphic phytoplankton and zooplankton populations. We also show that the coupling of spatial heterogeneity and migration results in the emergence of specific biogeographic patterns: (i) the emergence of a source-sink structure of the plankton metacommunities, (ii) changes in size diversity dependent on migratory intensity and on the scale at which diversity is considered (local vs. global), and (iii) the emergence of eco-evolutionary provinces (i.e., a spatial unit characterized by some level of abiotic heterogeneity but of homogenous size composition due to horizontal movements) at spatial scales that increase with the strength of the migratory processes.

The Size Dependence of Phytoplankton Growth Rates: A Trade-Off between Nutrient Uptake and Metabolism.

Rates of metabolism and population growth are often assumed to decrease universally with increasing organism size. Recent observations have shown, however, that maximum population growth rates among phytoplankton smaller than ∼6 µm in diameter tend to increase with organism size. Here we bring together observations and theory to demonstrate that the observed change in slope is attributable to a trade-off between nutrient uptake and the potential rate of internal metabolism. Specifically, we apply an established model of phytoplankton growth to explore a trade-off between the ability of cells to replenish their internal quota (which increases with size) and their ability to synthesize new biomass (which decreases with size). Contrary to the metabolic theory of ecology, these results demonstrate that rates of resource acquisition (rather than metabolism) provide the primary physiological constraint on the growth rates of some of the smallest and most numerically abundant photosynthetic organisms on Earth.

Crop Fertilization Impacts Epidemics and Optimal Latent Period of Biotrophic Fungal Pathogens.

Crop pathogens are known to rapidly adapt to agricultural practices. Although cultivar resistance breakdown and resistance to pesticides have been broadly studied, little is known about the adaptation of crop pathogens to fertilization regimes and no epidemiological model has addressed that question. However, this is a critical issue for developing sustainable low-input agriculture. In this article, we use a model of life history evolution of biotrophic wheat fungal pathogens in order to understand how they could adapt to changes in fertilization practices. We focus on a single pathogen life history trait, the latent period, which directly determines the amount of resources allocated to growth and reproduction along with the speed of canopy colonization. We implemented three fertilization scenarios, corresponding to major effects of increased nitrogen fertilization on crops: (i) increase in nutrient concentration in leaves, (ii) increase of leaf lifespan, and (iii) increase of leaf number (tillering) and size that leads to a bigger canopy size. For every scenario, we used two different fitness measures to identify putative evolutionary responses of latent period to changes in fertilization level. We observed that annual spore production increases with fertilization, because it results in more resources available to the pathogens. Thus, diminishing the use of fertilizers could reduce biotrophic fungal epidemics. We found a positive relationship between the optimal latent period and fertilization when maximizing total spore production over an entire season. In contrast, we found a negative relationship between the optimal latent period and fertilization when maximizing the within-season exponential growth rate of the pathogen. These contrasting results were consistent over the three tested fertilization scenarios. They suggest that between-strain diversity in the latent period, as has been observed in the field, may be due to diversifying selection in different cultural environments.

Pathogens trigger top-down climate forcing on ecosystem dynamics.

Evaluating the effects of climate variation on ecosystems is of paramount importance for our ability to forecast and mitigate the consequences of global change. However, the ways in which complex food webs respond to climate variations remain poorly understood. Here, we use long-term time series to investigate the effects of temperature variation on the intraguild-predation (IGP) system of Windermere (UK), a lake where pike (Esox lucius, top predator) feed on small-sized perch (Perca fluviatilis) but compete with large-sized perch for the same food sources. Spectral analyses of time series reveal that pike recruitment dynamics are temperature controlled. In 1976, expansion of a size-truncating perch pathogen into the lake severely impacted large perch and favoured pike as the IGP-dominant species. This pathogen-induced regime shift to a pike-dominated IGP apparently triggered a temperature-controlled trophic cascade passing through pike down to dissolved nutrients. In simple food chains, warming is predicted to strengthen top-down control by accelerating metabolic rates in ectothermic consumers, while pathogens of top consumers are predicted to dampen this top-down control. In contrast, the local IGP structure in Windermere made warming and pathogens synergistic in their top-down effects on ecosystem functioning. More generally, our results point to top predators as major mediators of community response to global change, and show that size-selective agents (e.g. pathogens, fishers or hunters) may change the topological architecture of food webs and alter whole ecosystem sensitivity to climate variation.

Interference versus exploitative competition in the regulation of size-structured populations.

Competition is a major regulatory factor in population and community dynamics. Its effects can be either direct in interference competition or indirect in exploitative competition. The impact of exploitative competition on population dynamics has been extensively studied from empirical and theoretical points of view, but the consequences of interference competition remain poorly understood. Here we study the effect of different levels of intraspecific interference competition on the dynamics of a size-structured population. We study a physiologically structured population model accounting for direct individual interactions, allowing for a gradient from exploitative competition to interference competition. We parameterize our model with data on experimental populations of the collembolan Folsomia candida. Our model predicts contrasting dynamics, depending on the level of interference competition. With low interference, our model predicts juvenile-driven generation cycles, but interference competition tends to dampen these cycles. With intermediate interference, giant individuals emerge and start dominating the population. Finally, strong interference competition causes a novel kind of adult-driven generation cycles referred to as interference-induced cycles. Our results shed new light on the interpretation of the size-structured dynamics of natural and experimental populations.

Population and life-history consequences of within-cohort individual variation.

The consequences of within-cohort (i.e., among-individual) variation for population dynamics are poorly understood, in particular for the case where life history is density dependent. We develop a physiologically structured population model that incorporates individual variation among and within cohorts and allows us to explore the intertwined relationship between individual life history and population dynamics. Our model is parameterized for the lizard Zootoca vivipara and reproduces well the species' dynamics and life history. We explore two common mechanisms that generate within-cohort variation: variability in food intake and variability in birth date. Predicted population dynamics are inherently very stable and do not qualitatively change when either of these sources of individual variation is introduced. However, increased within-cohort variation in food intake leads to changes in morphology, with longer but skinnier individuals, even though mean food intake does not change. Morphological changes result from a seemingly universal nonlinear relationship between growth and resource availability but may become apparent only in environments with strongly fluctuating resources. Overall, our results highlight the importance of using a mechanistic framework to gain insights into how different sources of intraspecific variability translate into life-history and population-dynamic changes.

Temperature-driven regime shifts in the dynamics of size-structured populations.

Global warming impacts virtually all biota and ecosystems. Many of these impacts are mediated through direct effects of temperature on individual vital rates. Yet how this translates from the individual to the population level is still poorly understood, hampering the assessment of global warming impacts on population structure and dynamics. Here, we study the effects of temperature on intraspecific competition and cannibalism and the population dynamical consequences in a size-structured fish population. We use a physiologically structured consumer-resource model in which we explicitly model the temperature dependencies of the consumer vital rates and the resource population growth rate. Our model predicts that increased temperature decreases resource density despite higher resource growth rates, reflecting stronger intraspecific competition among consumers. At a critical temperature, the consumer population dynamics destabilize and shift from a stable equilibrium to competition-driven generation cycles that are dominated by recruits. As a consequence, maximum age decreases and the proportion of younger and smaller-sized fish increases. These model predictions support the hypothesis of decreasing mean body sizes due to increased temperatures. We conclude that in size-structured fish populations, global warming may increase competition, favor smaller size classes, and induce regime shifts that destabilize population and community dynamics.

Stage-specific biomass overcompensation by juveniles in response to increased adult mortality in a wild fish population.

Recently developed theoretical models of stage-structured consumer-resource systems have shown that stage-specific biomass overcompensation can arise in response to increased mortality rates. We parameterized a stage-structured population model to simulate the effects of increased adult mortality caused by a pathogen outbreak in the perch (Perca fluviatilis) population of Windermere (UK) in 1976. The model predicts biomass overcompensation by juveniles in response to increased adult mortality due to a shift in food-dependent growth and reproduction rates. Considering cannibalism between life stages in the model reinforces this compensatory response due to the release from predation on juveniles at high mortality rates. These model predictions are matched by our analysis of a 60-year time series of scientific monitoring of Windermere perch, which shows that the pathogen outbreak induced a strong decrease in adult biomass and a corresponding increase in juvenile biomass. Age-specific adult fecundity and size at age were higher after than before the disease outbreak, suggesting that the pathogen-induced mortality released adult perch from competition, thereby increasing somatic and reproductive growth. Higher juvenile survival after the pathogen outbreak due to a release from cannibalism likely contributed to the observed biomass overcompensation. Our findings have general implications for predicting population- and community-level responses to increased size-selective mortality caused by exploitation or disease outbreaks.

Body downsizing caused by non-consumptive social stress severely depresses population growth rate.

Chronic social stress diverts energy away from growth, reproduction and immunity, and is thus a potential driver of population dynamics. However, the effects of social stress on demographic density dependence remain largely overlooked in ecological theory. Here we combine behavioural experiments, physiology and population modelling to show in a top predator (pike Esox lucius) that social stress alone may be a primary driver of demographic density dependence. Doubling pike density in experimental ponds under controlled prey availability did not significantly change prey intake by pike (i.e. did not significantly change interference or exploitative competition), but induced a neuroendocrine stress response reflecting a size-dependent dominance hierarchy, depressed pike energetic status and lowered pike body growth rate by 23 per cent. Assuming fixed size-dependent survival and fecundity functions parameterized for the Windermere (UK) pike population, stress-induced smaller body size shifts age-specific survival rates and lowers age-specific fecundity, which in Leslie matrices projects into reduced population rate of increase (lambda) by 37-56%. Our models also predict that social stress flattens elasticity profiles of lambda to age-specific survival and fecundity, thus making population persistence more dependent on old individuals. Our results suggest that accounting for non-consumptive social stress from competitors and predators is necessary to accurately understand, predict and manage food-web dynamics.

Allele fixation in a dynamic metapopulation: founder effects vs refuge effects.

The fixation of mutant alleles has been studied with models assuming various spatial population structures. In these models, the structure of the metapopulation that we call the "landscape" (number, size and connectivity of subpopulations) is often static. However, natural populations are subject to repetitive population size variations, fragmentation and secondary contacts at different spatiotemporal scales due to geological, climatic and ecological processes. In this paper, we examine how such dynamic landscapes can alter mutant fixation probability and time to fixation. We consider three stochastic landscape dynamics: (i) the population is subject to repetitive bottlenecks, (ii) to the repeated alternation of fragmentation and fusion of demes with a constant population carrying capacity, (iii) idem with a variable carrying capacity. We show by deriving a variance, a coalescent and a harmonic mean population effective size, and with simulations that these landscape dynamics generate repetitive founder effects which counteract selection, thereby decreasing the fixation probability of an advantageous mutant but accelerate fixation when it occurs. For models (ii) and (iii), we also highlight an antagonistic "refuge effect" which can strongly delay mutant fixation. The predominance of either founder effects or refuge effects determines the time to fixation and mainly depends on the characteristic time scales of the landscape dynamics.

The effect of population size and recombination on delayed evolution of polymorphism and speciation in sexual populations.

Recent theory suggests that absolute population size may qualitatively influence the outcome of evolution under disruptive selection in asexual populations. Large populations are predicted to undergo rapid evolutionary branching; however, in small populations, the waiting time to branching increases steeply with decreasing abundance, and below a critical size, the population remains monomorphic indefinitely. Here, we (1) extend the theory to sexual populations and (2) confront its predictions with empirical data, testing statistically whether lake size affects the level of resource polymorphism in arctic char (Salvelinus alpinus) in 22 lakes of different sizes. For a given level of recombination, our model predicts qualitatively similar relations between population size and time to evolutionary branching (either speciation or evolution of genetic polymorphism) as the asexual model, while recombination further increases the delay to branching. The loss of polymorphism at certain loci, an inherent aspect of multilocus-trait evolution, may increase the delay to speciation, resulting in stable genetic polymorphism without speciation. The empirical analysis demonstrates that the occurrence of resource polymorphism depends on both lake size and the number of coexisting fish species. For a given number of coexisting species, the level of polymorphism increases significantly with lake size, thus confirming our model prediction.

Stabilization of population fluctuations due to cannibalism promotes resource polymorphism in fish.

Resource polymorphism is a well-known phenomenon in many taxa, assumed to be a consequence of strong competition for resources and to be facilitated by stable environments and the presence of several profitable resources on which to specialize. In fish, resource polymorphism, in the form of planktivore-benthivore pairs, is found in a number of species. We gathered literature data on life-history characteristics and population dynamics for 15 fish species and investigated factors related to the presence of such resource polymorphism. This investigation indicated that early cannibalism and low overall population variability are typically associated with the presence of resource polymorphism. These findings match previously reported patterns of population dynamics for size-structured fish populations, whereby early cannibalism has been shown to decrease temporal variation in population dynamics and to equalize the profitability of the zooplankton and macroinvertebrate resources. Our study suggests that competition alone is not a sufficient condition for the development of resource polymorphism because overly strong competition is typically associated with increased temporal variation (environmental instability). We conclude that although resource competition is an important factor regulating the development of resource polymorphism, cannibalism may also play a fundamental role by dampening population oscillations and possibly by equalizing the profitability of different resources.

Food-dependent growth leads to overcompensation in stage-specific biomass when mortality increases: the influence of maturation versus reproduction regulation.

We analyze a stage-structured biomass model for size-structured consumer-resource interactions. Maturation of juvenile consumers is modeled with a food-dependent function that consistently translates individual-level assumptions about growth in body size to the population level. Furthermore, the model accounts for stage-specific differences in resource use and mortality between juvenile and adult consumers. Without such differences, the model reduces to the Yodzis and Innes (1992) bioenergetics model, for which we show that model equilibria are characterized by a symmetry property that reproduction and maturation are equally limited by food density. As a consequence, biomass production rate exactly equals loss rate through maintenance and mortality in each consumer stage. Stage-specific differences break up this symmetry and turn specific stages into net producers and others into net losers of biomass. As a consequence, the population in equilibrium can be regulated in two distinct ways: either through total population reproduction or through total population maturation as limiting process. In the case of reproduction regulation, increases in mortality may lead to an increase of juvenile biomass. In the case of maturation regulation, increases in mortality may increase adult biomass. This overcompensation in biomass occurs with increases in both stage-independent and stage-specific mortality, even when the latter targets the stage exhibiting overcompensation.

Alternative life-history pathways and the elasticity of stochastic matrix models.

Loop analysis is a powerful tool for analyzing matrix population models. This note shows that the results of loop analysis, which have been proved for constant matrices only, apply to stochastic matrices as well if elasticity is defined as the effect of a proportional perturbation of both mean and variance. Using the ideas of loop analysis, it is shown that the structure of the stochastic matrix in terms of alternative life-history pathways has important consequences for the effect of stochasticity on elasticities. If the life cycle contains nonoverlapping, alternative life-history pathways, the ranking in terms of elasticity of the most critical vital rates may be reversed in stochastic and the corresponding average environments. This has obvious and important consequences for population management because focusing on a deterministic model would lead to an ineffective or counterproductive management strategy.

When everything is not everywhere but species evolve: an alternative method to model adaptive properties of marine ecosystems.

The functional and taxonomic biogeography of marine microbial systems reflects the current state of an evolving system. Current models of marine microbial systems and biogeochemical cycles do not reflect this fundamental organizing principle. Here, we investigate the evolutionary adaptive potential of marine microbial systems under environmental change and introduce explicit Darwinian adaptation into an ocean modelling framework, simulating evolving phytoplankton communities in space and time. To this end, we adopt tools from adaptive dynamics theory, evaluating the fitness of invading mutants over annual timescales, replacing the resident if a fitter mutant arises. Using the evolutionary framework, we examine how community assembly, specifically the emergence of phytoplankton cell size diversity, reflects the combined effects of bottom-up and top-down controls. When compared with a species-selection approach, based on the paradigm that "Everything is everywhere, but the environment selects", we show that (i) the selected optimal trait values are similar; (ii) the patterns emerging from the adaptive model are more robust, but (iii) the two methods lead to different predictions in terms of emergent diversity. We demonstrate that explicitly evolutionary approaches to modelling marine microbial populations and functionality are feasible and practical in time-varying, space-resolving settings and provide a new tool for exploring evolutionary interactions on a range of timescales in the ocean.

Dwarfs and Giants: Cannibalism and Competition in Size-Structured Populations.

Cannibals and their victims often share common resources and thus potentially compete. Smaller individuals are often competitively superior to larger ones because of size-dependent scaling of foraging and metabolic rates, while larger ones may use cannibalism to counter this competition. We study the interplay between cannibalism and competition using a size-structured population model in which all individuals consume a shared resource but in which larger ones may cannibalize smaller conspecifics. In this model, intercohort competition causes single-cohort cycles when cannibalism is absent. Moderate levels of cannibalism reduce intercohort competition, enabling coexistence of many cohorts. More voracious cannibalism, in combination with competition, produces large-amplitude cycles and a bimodal population size distribution with many small and few giant individuals. These coexisting ``dwarfs'' and ``giants'' have very different life histories, resulting from a reversal in importance of cannibalism and competition. The population structure at time of birth determines whether individuals suffer severe cannibalism, with the few survivors reaching giant sizes, or whether they suffer intense intracohort competition, with all individuals remaining small. These model results agree remarkably well with empirical data on perch population dynamics. We argue that the induction of cannibalistic giants in piscivorous fish is a population-dynamic emergent phenomenon that requires a combination of size-dependent cannibalism and competition.

Population dynamic theory of size-dependent cannibalism.

Cannibalism is characterized by four aspects: killing victims, gaining energy from victims, size-dependent interactions and intraspecific competition. In this review of mathematical models of cannibalistic populations, we relate the predicted population dynamic consequences of cannibalism to its four defining aspects. We distinguish five classes of effects of cannibalism: (i) regulation of population size; (ii) destabilization resulting in population cycles or chaos; (iii) stabilization by damping population cycles caused by other interactions; (iv) bistability such that, depending on the initial conditions, the population converges to one of two possible stable states; and (v) modification of the population size structure. The same effects of cannibalism may be caused by different combinations of aspects of cannibalism. By contrast, the same combination of aspects may lead to different effects. For particular cannibalistic species, the consequences of cannibalism will depend on the presence and details of the four defining aspects. Empirical evidence for the emerged theory of cannibalism is discussed briefly. The implications of the described dynamic effects of cannibalism are discussed in the context of community structure, making a comparison with the community effects of intraguild predation.