High importance of indirect evolutionary rescue in a small food web.

Evolutionary rescue may allow species to survive environmental change, but how this mechanism operates in food webs is poorly understood. Here, the evolutionary rescue was investigated in a small model food web, systematically allowing the evolution of each single species in order to reveal how its adaptation affects the persistence of itself and others. The impact of evolution was highly species-specific and not necessarily positive: only one species, the specialist predator, consistently had a positive impact on overall persistence. Most strikingly, evolution overwhelmingly affected other species: rescue of others (indirect rescue) was far more frequent than self-rescue, and negative effects were nearly always indirect. This demonstrates that evolutionary rescue in food webs is inextricably bound up with species interactions, as the effects of evolution in one species ripple through the entire community. It is therefore critically important to consider the food web context in efforts to understand how species may survive global change.

Shifts from cooperative to individual-based predation defense determine microbial predator-prey dynamics.

Predation defense is an important feature of predator-prey interactions adding complexity to ecosystem dynamics. Prey organisms have developed various strategies to escape predation which differ in mode (elude vs. attack), reversibility (inducible vs. permanent), and scope (individual vs. cooperative defenses). While the mechanisms and controls of many singular defenses are well understood, important ecological and evolutionary facets impacting long-term predator-prey dynamics remain underexplored. This pertains especially to trade-offs and interactions between alternative defenses occurring in prey populations evolving under predation pressure. Here, we explored the dynamics of a microbial predator-prey system consisting of bacterivorous flagellates (Poteriospumella lacustris) feeding on Pseudomonas putida. Within five weeks of co-cultivation corresponding to about 35 predator generations, we observed a consistent succession of bacterial defenses in all replicates (n = 16). Initially, bacteria expressed a highly effective cooperative defense based on toxic metabolites, which brought predators close to extinction. This initial strategy, however, was consistently superseded by a second mechanism of predation defense emerging via de novo mutations. Combining experiments with mathematical modeling, we demonstrate how this succession of defenses is driven by the maximization of individual rather than population benefits, highlighting the role of rapid evolution in the breakdown of social cooperation.

The double-edged sword of inducible defences: costs and benefits of maladaptive switching from the individual to the community level.

Phenotypic plasticity can increase individual fitness when environmental conditions change over time. Inducible defences are a striking example, allowing species to react to fluctuating predation pressure by only expressing their costly defended phenotype under high predation risk. Previous theoretical investigations have focused on how this affects predator-prey dynamics, but the impact on competitive outcomes and broader community dynamics has received less attention. Here we use a small food web model, consisting of two competing plastic autotrophic species exploited by a shared consumer, to study how the speed of inducible defences across three trade-off constellations affects autotroph coexistence, biomasses across trophic levels, and temporal variability. Contrary to the intuitive idea that faster adaptation increases autotroph fitness, we found that higher switching rates reduced individual fitness as it consistently provoked more maladaptive switching towards undefended phenotypes under high predation pressure. This had an unexpected positive impact on the consumer, increasing consumer biomass and lowering total autotroph biomass. Additionally, maladaptive switching strongly reduced autotroph coexistence through an emerging source-sink dynamic between defended and undefended phenotypes. The striking impact of maladaptive switching on species and food web dynamics indicates that this mechanism may be of more critical importance than previously recognized.

Predator coexistence through emergent fitness equalization.

The competitive exclusion principle is one of the oldest ideas in ecology and states that without additional self-limitation two predators cannot coexist on a single prey. The search for mechanisms allowing coexistence despite this has identified niche differentiation between predators as crucial: without this, coexistence requires the predators to have exactly the same R* values, which is considered impossible. However, this reasoning misses a critical point: predators' R* values are not static properties, but affected by defensive traits of their prey, which in turn can adapt in response to changes in predator densities. Here I show that this feedback between defense and predator dynamics enables stable predator coexistence without ecological niche differentiation. Instead, the mechanism driving coexistence is that prey adaptation causes defense to converge to the value where both predators have equal R* values ("fitness equalization"). This result is highly general, independent of specific model details, and applies to both rapid defense evolution and inducible defenses. It demonstrates the importance of considering long-standing ecological questions from an eco-evolutionary viewpoint, and showcases how the effects of adaptation can cascade through communities, driving diversity on higher trophic levels. These insights offer an important new perspective on coexistence theory.

Co-adaptation impacts the robustness of predator-prey dynamics against perturbations.

Global change threatens the maintenance of ecosystem functions that are shaped by the persistence and dynamics of populations. It has been shown that the persistence of species increases if they possess larger trait adaptability. Here, we investigate whether trait adaptability also affects the robustness of population dynamics of interacting species and thereby shapes the reliability of ecosystem functions that are driven by these dynamics. We model co-adaptation in a predator-prey system as changes to predator offense and prey defense due to evolution or phenotypic plasticity. We investigate how trait adaptation affects the robustness of population dynamics against press perturbations to environmental parameters and against pulse perturbations targeting species abundances and their trait values. Robustness of population dynamics is characterized by resilience, elasticity, and resistance. In addition to employing established measures for resilience and elasticity against pulse perturbations (extinction probability and return time), we propose the warping distance as a new measure for resistance against press perturbations, which compares the shapes and amplitudes of pre- and post-perturbation population dynamics. As expected, we find that the robustness of population dynamics depends on the speed of adaptation, but in nontrivial ways. Elasticity increases with speed of adaptation as the system returns more rapidly to the pre-perturbation state. Resilience, in turn, is enhanced by intermediate speeds of adaptation, as here trait adaptation dampens biomass oscillations. The resistance of population dynamics strongly depends on the target of the press perturbation, preventing a simple relationship with the adaptation speed. In general, we find that low robustness often coincides with high amplitudes of population dynamics. Hence, amplitudes may indicate the robustness against perturbations also in other natural systems with similar dynamics. Our findings show that besides counteracting extinctions, trait adaptation indeed strongly affects the robustness of population dynamics against press and pulse perturbations.

Modelling inducible defences in predator-prey interactions: assumptions and dynamical consequences of three distinct approaches.

Inducible defences against predation are widespread in the natural world, allowing prey to economise on the costs of defence when predation risk varies over time or is spatially structured. Through interspecific interactions, inducible defences have major impacts on ecological dynamics, particularly predator-prey stability and phase lag. Researchers have developed multiple distinct approaches, each reflecting assumptions appropriate for particular ecological communities. Yet, the impact of inducible defences on ecological dynamics can be highly sensitive to the modelling approach used, making the choice of model a critical decision that affects interpretation of the dynamical consequences of inducible defences. Here, we review three existing approaches to modelling inducible defences: Switching Function, Fitness Gradient and Optimal Trait. We assess when and how the dynamical outcomes of these approaches differ from each other, from classic predator-prey dynamics and from commonly observed eco-evolutionary dynamics with evolving, but non-inducible, prey defences. We point out that the Switching Function models tend to stabilise population dynamics, and the Fitness Gradient models should be carefully used, as the difference with evolutionary dynamics is important. We discuss advantages of each approach for applications to ecological systems with particular features, with the goal of providing guidelines for future researchers to build on.

Reversed predator-prey cycles are driven by the amplitude of prey oscillations.

Ecoevolutionary feedbacks in predator-prey systems have been shown to qualitatively alter predator-prey dynamics. As a striking example, defense-offense coevolution can reverse predator-prey cycles, so predator peaks precede prey peaks rather than vice versa. However, this has only rarely been shown in either model studies or empirical systems. Here, we investigate whether this rarity is a fundamental feature of reversed cycles by exploring under which conditions they should be found. For this, we first identify potential conditions and parameter ranges most likely to result in reversed cycles by developing a new measure, the effective prey biomass, which combines prey biomass with prey and predator traits, and represents the prey biomass as perceived by the predator. We show that predator dynamics always follow the dynamics of the effective prey biomass with a classic »-phase lag. From this key insight, it follows that in reversed cycles (i.e., ¾-lag), the dynamics of the actual and the effective prey biomass must be in antiphase with each other, that is, the effective prey biomass must be highest when actual prey biomass is lowest, and vice versa. Based on this, we predict that reversed cycles should be found mainly when oscillations in actual prey biomass are small and thus have limited impact on the dynamics of the effective prey biomass, which are mainly driven by trait changes. We then confirm this prediction using numerical simulations of a coevolutionary predator-prey system, varying the amplitude of the oscillations in prey biomass: Reversed cycles are consistently associated with regions of parameter space leading to small-amplitude prey oscillations, offering a specific and highly testable prediction for conditions under which reversed cycles should occur in natural systems.

Disentangling eco-evolutionary dynamics of predator-prey coevolution: the case of antiphase cycles.

The impact of rapid predator-prey coevolution on predator-prey dynamics remains poorly understood, as previous modelling studies have given rise to contradictory conclusions and predictions. Interpreting and reconciling these contradictions has been challenging due to the inherent complexity of model dynamics, defying mathematical analysis and mechanistic understanding. We develop a new approach here, based on the Geber method for deconstructing eco-evolutionary dynamics, for gaining such understanding. We apply this approach to a co-evolutionary predator-prey model to disentangle the processes leading to either antiphase or »-lag cycles. Our analysis reveals how the predator-prey phase relationship is driven by the temporal synchronization between prey biomass and defense dynamics. We further show when and how prey biomass and trait dynamics become synchronized, resulting in antiphase cycles, allowing us to explain and reconcile previous modelling and empirical predictions. The successful application of our proposed approach provides an important step towards a comprehensive theory on eco-evolutionary feedbacks in predator-prey systems.

Grazing resistance of bacterial biofilms: a matter of predators' feeding trait.

Biofilm formation in bacteria is considered to be one strategy to avoid protozoan grazing. However, this assumption is largely based on experiments with suspension-feeding protozoans. Here we test the hypothesis that grazing resistance depends on both the grazers' feeding trait and the bacterial phenotype, rather than being a general characteristic of bacterial biofilms. We combined batch experiments with mathematical modelling, considering the bacterium Pseudomonas putida and either a suspension-feeding (i.e. the ciliate Paramecium tetraurelia) or a surface-feeding grazer (i.e. the amoeba Acanthamoeba castellanii). We find that both plankton and biofilm phenotypes were consumed, when exposed to their specialised grazer, whereas the other phenotype remained grazing-resistant. This was consistently shown in two experiments (starting with either only planktonic bacteria or with additional pre-grown biofilms) and matches model predictions. In the experiments, the plankton feeder strongly stimulated the biofilm biomass. This stimulation of the resistant prey phenotype was not predicted by the model and it was not observed for the biofilm feeders, suggesting the existence of additional mechanisms that stimulate biofilm formation besides selective feeding. Overall, our results confirm our hypothesis that grazing resistance is a matter of the grazers' trait (i.e. feeding type) rather than a biofilm-specific property.

The Role of Within-Host Competition for Coexistence in Multiparasitoid-Host Systems.

Multiparasitism (females of multiple species parasitizing the same host) is a ubiquitous phenomenon in parasitoids, yet the role of within-host competition has been mostly ignored in multiparasitoid-host models. Here we study the effect of varying the degree of competition at different life stages: competition over oviposition sites (between-adult competition) and larval competition over resources within the host (within-host competition). We adapt a Nicholson-Bailey model to allow for varying levels of between-adult competition (varying the overlap in species distributions) and within-host competition (varying the number of offspring that can successfully emerge from a host). Surprisingly, while stronger between-adult competition reduces coexistence, stronger within-host competition promotes it. Asymmetric between-adult competition (a fecundity difference between the two species) reduces coexistence when compared to symmetric competition; this can be counteracted by asymmetric within-host competition (within-host competitive advantage of the lower-fecundity species), but only when within-host competition is strong and the correlation between the parasitoids' distributions is intermediate. We discuss our results in the context of the interaction between two parasitoid species, Nasonia vitripennis and Nasonia giraulti, which have strongly correlated distributions and high levels of multiparasitism in the field. We conclude that either low or asymmetric within-host competition is unlikely to explain their coexistence.

The importance of ecological costs for the evolution of plant defense against herbivory.

Plant defense against herbivory comes at a cost, which can be either direct (reducing resources available for growth and reproduction) or indirect (through reducing ecological performance, for example intraspecific competitiveness). While direct costs have been well studied in theoretical models, ecological costs have received almost no attention. In this study we compare models with a direct trade-off (reduced growth rate) to models with an ecological trade-off (reduced competitive ability), using a combination of adaptive dynamics and simulations. In addition, we study the dependence of the level of defense that can evolve on the type of defense (directly by reducing consumption, or indirectly by inducing herbivore mortality (toxicity)), and on the type of herbivore against which the plant is defending itself (generalists or specialists). We find three major results: First, for both direct and ecological costs, defense only evolves if the benefit to the plant is direct (through reducing consumption). Second, the type of cost has a major effect on the evolutionary dynamics: direct costs always lead to a single optimal strategy against herbivores, but ecological costs can lead to branching and the coexistence of non-defending and defending plants; however, coexistence is only possible when defending against generalist herbivores. Finally, we find that fast-growing plants invest less than slow-growing plants when defending against generalist herbivores, as predicted by the Resource Availability Hypothesis, but invest more than slow-growing plants when defending against specialists. Our results clearly show that assumptions about ecological interactions are crucial for understanding the evolution of defense against herbivores.

The effect of cryptic female choice on sex allocation in simultaneous hermaphrodites.

Sex allocation theory for simultaneous hermaphrodites has focused primarily on the effects of sperm competition, but the role of mate choice has so far been neglected. We present a model to study the coevolution of cryptic female choice and sex allocation in simultaneous hermaphrodites. We show that the mechanism of cryptic female choice has a strong effect on the evolutionary outcome: if individuals remove a fixed proportion of less-preferred sperm, the optimal sex allocation is more female biased (i.e. more biased towards egg production) than without cryptic female choice; conversely, if a fixed amount of sperm is removed, sex allocation is less female-biased than without cryptic female choice, and can easily become male biased (i.e. biased towards sperm production). Under male-biased sex allocation, hermaphroditism can become unstable and the population can split into pure males and hermaphrodites with a female-biased allocation. We discuss the idea that the evolution of sex allocation may depend on the outcome of sexual conflict over the fate of received sperm: the sperm donor may attempt to manipulate or by-pass cryptic female choice and the sperm recipient is expected to resist such manipulation. We conclude that cryptic female choice can have a strong influence on sex allocation in simultaneous hermaphrodites and strongly encourage empirical work on this question.