Pulsed-resource dynamics constrain the evolution of predator-prey interactions

Although temporal variability in the physical environment plays a major role in population fluctuations, little is known about how it drives the ecological and evolutionary dynamics of species interactions. We studied experimentally how extrinsic resource pulses affect evolutionary and ecological dynamics between the prey bacterium Serratia marcescens and the predatory protozoan Tetrahymena thermophila. Predation increased the frequency of defensive, nonpigmented prey types, which bore competitive costs in terms of reduced maximum growth rate, most in a constant-resource environment. Furthermore, the predator densities of the pulsed-resource environment regularly fluctuated above and below the mean predator densities of the constant environment. These results suggest that selection favored fast-growing competitor prey types over defensive but slower-growing prey types more often in the pulsed-resource environment (abundance of resources and low predation risk). As a result, the selection for prey defense fluctuated more in the pulsed-resource environment, leading to a weaker mean response in prey defense. At the ecological level, the evolution of prey defense weakened the relative strength of top-down regulation on prey community. This was more evident in the constant-resource environment, whereas the slow emergence of defensive prey types gradually decreased the amplitude of predator peaks in the pulsed-resource environment. Our study suggests that rapid evolution plays a smaller role in the ecological dynamics of communities dominated by resource pulses.     

ECOLOGICAL CONDITIONS AFFECT EVOLUTIONARY TRAJECTORY IN A PREDATOR–PREY SYSTEM

The arms race of adaptation and counter adaptation in predator–prey interactions is a fascinating evolutionary dynamic with many consequences, including local adaptation and the promotion or maintenance of diversity. Although such antagonistic coevolution is suspected to be widespread in nature, experimental documentation of the process remains scant, and we have little understanding of the impact of ecological conditions. Here, we present evidence of predator–prey coevolution in a long-term experiment involving the predatory bacterium Bdellovibrio bacteriovorus and the prey Pseudomonas fluorescens , which has three morphs (SM, FS, and WS). Depending on experimentally applied disturbance regimes, the predator–prey system followed two distinct evolutionary trajectories, where the prey evolved to be either super-resistant to predation (SM morph) without counter-adaptation by the predator, or moderately resistant (FS morph), specialized to and coevolving with the predator. Although predation-resistant FS morphs suffer a cost of resistance, the evolution of extreme resistance to predation by the SM morph was apparently unconstrained by other traits (carrying capacity, growth rate). Thus we demonstrate empirically that ecological conditions can shape the evolutionary trajectory of a predator–prey system.     

Contemporary evolution and genetic change of prey as a response to predator removal

The ecological effects of predator removal and its consequence on prey behavior have been investigated widely; however, predator removal can also cause contemporary evolution of prey resulting in prey genetic change. Here we tested the role of predator removal on the contemporary evolution of prey traits such as movement, reproduction and foraging. We use EcoSim simulation which allows complex intra- and inter-specific interactions, based on individual evolving behavioral models, as well as complex predator–prey dynamics and coevolution in spatially homogenous and heterogeneous worlds. We model organisms' behavior using fuzzy cognitive maps (FCM) that are coded in their genomes which has a clear semantics making reasoning about causality of any evolved behavior possible. We show that the contemporary evolution of prey behavior owing to predator removal is also accompanied by prey genetic change. We employed machine learning methods, now recognized as holding great promise for the advancement of our understanding and prediction of ecological phenomena. A classification algorithm was used to demonstrate the difference between genomes belonging to prey coevolving with predators and prey evolving in the absence of predation pressure. We argue that predator introductions to naive prey might be destabilizing if prey have evolved and adapted to the absence of predators. Our results suggest that both predator introductions and predator removal from an ecosystem have widespread effects on the survival and evolution of prey by altering their genomes and behavior, even after relatively short time intervals. Our study highlights the need to consider both ecological and evolutionary time scales, as well as the complex interplay of behaviors between trophic levels, in determining the outcomes of predator–prey interactions.     

ORGANIZATION OF PREDATOR-PREY COMMUNITIES AS AN EVOLUTIONARY GAME

We consider a simple predator-prey model of coevolution. By allowing coevolution both within and between trophic levels the model breaks the traditional dichotomy between coevolution among competitors and coevolution between a prey and its predator. By allowing the diversity of prey and predator species to emerge as a property of the evolutionarily stable strategies (ESS), the model breaks another constraint of most approaches to coevolution that consider as fixed the number of coevolving species. The number of species comprising the ESS is influenced by a parameter that determines the predator's niche breadth. Depending upon the parameter's value the ESS may contain: 1) one prey and one predator species, 2) two prey and one predator, 3) two prey and two predators, 4) three prey and two predators, 5) three prey and three predators, etc. Evolutionarily, these different ESSs all emerge from the same model. Ecologically, however, these ESSs result in very different patterns of community organization. In some communities the predator species are ecologically keystone in that their removal results in extinctions among the prey species. In others, the removal of a predator species has no significant impact on the prey community. These varied ecological roles for the predator species contrasts sharply with the essential evolutionary role of the predators in promoting prey species diversity. The ghost of predation past in which a predator's insignificant ecological role obscures its essential evolutionary role may be a frequent property of communities of predator and prey.     

Eco‐evolutionary feedback promotes Red Queen dynamics and selects for sex in predator populations

Although numerous hypotheses exist to explain the overwhelming presence of sexual reproduction across the tree of life, we still cannot explain its prevalence when considering all inherent costs involved. The Red Queen hypothesis states that sex is maintained because it can create novel genotypes with a selective advantage. This occurs when the interactions between species induce frequent environmental change. Here, we investigate whether coevolution and eco‐evolutionary feedback dynamics in a predator‐prey system allows for indirect selection and maintenance of sexual reproduction in the predator. Combining models and chemostat experiments of a rotifer‐algae system we show a continuous feedback between population and trait change along with recurrent shifts from selection by predation and competition for a limited resource. We found that a high propensity for sex was indirectly selected and was maintained in rotifer populations within environments containing these eco‐evolutionary dynamics; whereas within environments under constant conditions, predators evolved rapidly to lower levels of sex. Thus, our results indicate that the influence of eco‐evolutionary feedback dynamics on the overall evolutionary change has been underestimated.     

Not attackable or not crackable—How pre‐ and post‐attack defenses with different competition costs affect prey coexistence and population dynamics

It is well‐known that prey species often face trade‐offs between defense against predation and competitiveness, enabling predator‐mediated coexistence. However, we lack an understanding of how the large variety of different defense traits with different competition costs affects coexistence and population dynamics. Our study focusses on two general defense mechanisms, that is, pre‐attack (e.g., camouflage) and post‐attack defenses (e.g., weaponry) that act at different phases of the predator—prey interaction. We consider a food web model with one predator, two prey types and one resource. One prey type is undefended, while the other one is pre‐ or post‐attack defended paying costs either by a higher half‐saturation constant for resource uptake or a lower maximum growth rate. We show that post‐attack defenses promote prey coexistence and stabilize the population dynamics more strongly than pre‐attack defenses by interfering with the predator's functional response: Because the predator spends time handling “noncrackable” prey, the undefended prey is indirectly facilitated. A high half‐saturation constant as defense costs promotes coexistence more and stabilizes the dynamics less than a low maximum growth rate. The former imposes high costs at low resource concentrations but allows for temporally high growth rates at predator‐induced resource peaks preventing the extinction of the defended prey. We evaluate the effects of the different defense mechanisms and costs on coexistence under different enrichment levels in order to vary the importance of bottom‐up and top‐down control of the prey community.     

The effects of interacting species on predator-prey coevolution

Simple optimization models are used to explore the effects that an additional species has on predator-prey coevolution. The additional species is either an alternative prey or a higher-level predator that consumes the first predator species. Results indicate that a variety of effects on predator-prey coevolution are possible. In general, the additional species does not decouple evolutionary changes in the predator and the prey, and often leads to stronger coupling. The manner in which predator and prey adaptations combine to determine the predator's capture rate has a major effect on how an additional species influences the coevolutionary responses of the original pair of species.     

Chaotic Red Queen coevolution in three-species food chains

Coevolution between two antagonistic species follows the so-called ‘Red Queen dynamics’ when reciprocal selection results in an endless series of adaptation by one species and counteradaptation by the other. Red Queen dynamics are ‘genetically driven’ when selective sweeps involving new beneficial mutations result in perpetual oscillations of the coevolving traits on the slow evolutionary time scale. Mathematical models have shown that a prey and a predator can coevolve along a genetically driven Red Queen cycle. We found that embedding the prey–predator interaction into a three-species food chain that includes a coevolving superpredator often turns the genetically driven Red Queen cycle into chaos. A key condition is that the prey evolves fast enough. Red Queen chaos implies that the direction and strength of selection are intrinsically unpredictable beyond a short evolutionary time, with greatest evolutionary unpredictability in the superpredator. We hypothesize that genetically driven Red Queen chaos could explain why many natural populations are poised at the edge of ecological chaos. Over space, genetically driven chaos is expected to cause the evolutionary divergence of local populations, even under homogenizing environmental fluctuations, and thus to promote genetic diversity among ecological communities over long evolutionary time.     

Asymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie

BACKGROUND: Coevolution between pairs of antagonistic species is generally considered an endless "arms race" between attack and defense traits to counteract the adaptive responses of the other species. PRESENTATION OF THE HYPOTHESIS: When more than two species are involved, diffuse coevolution of hosts and parasitoids could be asymmetric because consumers can choose their prey whereas preys do not choose their predator. This asymmetry may lead to differences in the rate of evolution of the antagonistic species in response to selection. The more long-standing the coevolution of a given pair of antagonistic populations, the higher should be the fitness advantage for the consumer. Therefore, the main prediction of the hypothesis is that the consumer trophic level is more likely to win the coevolution race. TESTING THE HYPOTHESIS: We propose testing the asymmetry hypothesis by focusing on the tritrophic system plant/aphid/aphid parasitoid. The analysis of the genetic variability in the virulence of several parasitoid populations and in the defenses of several aphid species or several clones of the same aphid species could be compared. Moreover, the analysis of the neutral population genetic structure of the parasitoid as a function of the aphid host, the plant host and geographic isolation may complement the detection of differences between host and parasitoid trophic specialization. IMPLICATIONS OF THE HYPOTHESIS: Genetic structures induced by the arms race between antagonistic species may be disturbed by asymmetry in coevolution, producing neither rare genotype advantages nor coevolutionary hotspots. Thus this hypothesis profoundly changes our understanding of coevolution and may have important implications in terms of pest management.     

Rapidly fluctuating environments constrain coevolutionary arms races by impeding selective sweeps

Although pervasive, the impact of temporal environmental heterogeneity on coevolutionary processes is poorly understood. Productivity is a key temporally heterogeneous variable, and increasing productivity has been shown to increase rates of antagonistic arms race coevolution, and lead to the evolution of more broadly resistant hosts and more broadly infectious parasites. We investigated the effects of the grain of environmental heterogeneity, in terms of fluctuations in productivity, on bacteria–phage coevolution. Our findings demonstrate that environmental heterogeneity could constrain antagonistic coevolution, but that its effect was dependent upon the grain of heterogeneity, such that both the rate and extent of coevolution were most strongly limited in fine-grained, rapidly fluctuating heterogeneous environments. We further demonstrate that rapid environmental fluctuations were likely to have impeded selective sweeps of resistance alleles, which occurred over longer durations than the fastest, but not the slowest, frequency of fluctuations used. Taken together our results suggest that fine-grained environmental heterogeneity constrained the coevolutionary arms race by impeding selective sweeps.     

Handling time promotes the coevolution of aggregation in predator-prey systems

Predators often have type II functional responses and live in environments where their life history traits as well as those of their prey vary from patch to patch. To understand how spatial heterogeneity and predator handling times influence the coevolution of patch preferences and ecological stability, we perform an ecological and evolutionary analysis of a Nicholson-Bailey type model. We prove that coevolutionarily stable prey and searching predators prefer patches that in isolation support higher prey and searching predator densities, respectively. Using this fact, we determine how environmental variation and predator handling times influence the spatial patterns of patch preferences, population abundances and per-capita predation rates. In particular, long predator handling times are shown to result in the coevolution of predator and prey aggregation. An analytic expression characterizing ecological stability of the coevolved populations is derived. This expression implies that contrary to traditional theoretical expectations, predator handling time can stabilize predator-prey interactions through its coevolutionary influence on patch preferences. These results are shown to have important implications for classical biological control.     

Innate threat-sensitive foraging: black-tailed deer remain more fearful of wolf than of the less dangerous black bear even after 100 years of wolf absence

Anti-predator behaviors often entail foraging costs, and thus prey response to predator cues should be adjusted to the level of risk (threat-sensitive foraging). Simultaneously dangerous predators (with high hunting success) should engender the evolution of innate predator recognition and appropriate anti-predator behaviors that are effective even upon the first encounter with the predator. The above leads to the prediction that prey might respond more strongly to cues of dangerous predators that are absent, than to cues of less dangerous predators that are actually present. In an applied context this would predict an immediate and stronger response of ungulates to the return of top predators such as wolves (Canis lupus) in many parts of Europe and North America than to current, less threatening, mesopredators. We investigated the existence of innate threat-sensitive foraging in black-tailed deer. We took advantage of a quasi-experimental situation where deer had not experienced wolf predation for ca. 100 years, and were only potentially exposed to black bears (Ursus americanus). We tested the response of deer to the urine of wolf (dangerous) and black bear (less dangerous). Our results support the hypothesis of innate threat-sensitive foraging with clear increased passive avoidance and olfactory investigation of cues from wolf, and surprisingly none to black bear. Prey which have previously evolved under high risk of predation by wolves may react strongly to the return of wolf cues in their environments thanks to innate responses retained during the period of predator absence, and this could be the source of far stronger non-consumptive effects of the predator guild than currently observed.     

A meta‐analysis of non‐consumptive predator effects in arthropods: the influence of organismal and environmental characteristics

Non‐consumptive effects (NCEs) – changes in prey behavior or physiology in response to predator threat – are common and can be as strong as consumptive effects. However, our knowledge of NCEs in arthropod systems is lacking. Factors related to study organism and environment have the potential to influence the occurrence and magnitude of NCEs in arthropod systems. While factors such as coevolutionary history of natural enemies and their prey, predator cue, predator or prey feeding mode, and refuge availability have been theoretically and empirically examined, no trends have been proposed for arthropods. We compiled 62 studies, yielding 128 predator–prey interactions, which explicitly examined NCEs in experiments where arthropods were identified to species, using a previously published database of papers from 1990 to 2005 and a new database of papers published from 2006 to 2015. Using these data, we conducted a meta‐analysis to explore the influence of organismal and environmental characteristics on the magnitude of predator NCEs. Our analysis addressed the following three questions. 1) Does predator–prey coevolution give rise to stronger NCEs than when predator and prey species did not coevolve? 2) What influence does habitat type and refuge availability have on NCEs? 3) How do predator characteristics (cue type, hunting mode and life stage) and prey characteristics (mobility, life stage, specialization, gregariousness and feeding mode) influence NCEs? We found that while NCEs were similar across most measured characteristics, NCEs on prey activity were significantly stronger when predator and prey shared an evolutionary history. Our results support growing evidence that NCEs have a negative effect on prey traits and that behavioral NCEs are stronger than physiological ones. Additional studies are needed to be confident in any emerging patterns, therefore we identify key gaps in the literature on NCEs in arthropod systems and discuss ideas for moving forward.     

Antagonistic coevolution across productivity gradients: an experimental test of the effects of dispersal

Coevolution commonly occurs in spatially heterogeneous environments, resulting in variable selection pressures acting on coevolving species. Dispersal across such environments is predicted to have a major impact on local coevolutionary dynamics. Here, we address how co‐dispersal of coevolving populations of host and parasite across an environmental productivity gradient affected coevolution in experimental populations of bacteria and their parasitic viruses (phages). The rate of coevolution between bacteria and phages was greater in high‐productivity environments. High‐productivity immigrants (～2% of the recipient population) caused coevolutionary dynamics (rates of coevolution and degree of generalist evolution) in low‐productivity environments to be largely indistinguishable from high‐productivity environments, whereas immigration from low‐productivity environments (～0.5% of the population) had no discernable impact. These results could not be explained by demography alone, but rather high‐productivity immigrants had a selective advantage in low‐productivity environments, but not vice versa. Coevolutionary interactions in high‐productivity environments are therefore likely to have a disproportionate impact on coevolution across the landscape as a whole.     

Introduced species provide a novel temporal resource that facilitates native predator population growth

Non-native species are recognized as important components of change to food web structure. Non-native prey may increase native predator populations by providing an additional food source and simultaneously decrease native prey populations by outcompeting them for a limited resource. This pattern of apparent competition may be important for plants and sessile marine invertebrate suspension feeders as they often compete for space and their immobile state make them readily accessible to predators. Reported studies on apparent competition have rarely been examined in biological invasions and no study has linked seasonal patterns of native and non-native prey abundance to increasing native predator populations. Here, we evaluate the effects of non-native colonial ascidians (Diplosoma listerianum and Didemnum vexillum) on population growth of a native predator (bloodstar, Henricia sanguinolenta) and native sponges through long-term surveys of abundance, prey choice and growth experiments. We show non-native species facilitate native predator population growth by providing a novel temporal resource that prevents loss of predator biomass when its native prey species are rare. We expect that by incorporating native and non-native prey seasonal abundance patterns, ecologists will gain a more comprehensive understanding of the mechanisms underlying the effects of non-native prey species on native predator and prey population dynamics.     

Dynamics and responses to mortality rates of competing predators undergoing predator-prey cycles

Two or more competing predators can coexist using a single homogeneous prey species if the system containing all three undergoes internally generated fluctuations in density. However, the dynamics of species that coexist via this mechanism have not been extensively explored. Here, we examine both the nature of the dynamics and the responses of the mean densities of each predator to mortality imposed upon it or its competitor. The analysis of dynamics uncovers several previously undescribed behaviors for this model, including chaotic fluctuations, and long-term transients that differ significantly from the ultimate patterns of fluctuations. The limiting dynamics of the system can be loosely classified as synchronous cycles, asynchronous cycles, and chaotic dynamics. Synchronous cycles are simple limit cycles with highly positively correlated densities of the two predator species. Asynchronous cycles are limit cycles, frequently of complex form, including a significant period during which prey density is nearly constant while one predator gradually, monotonically replaces the other. Chaotic dynamics are aperiodic and generally have intermediate correlations between predator densities. Continuous changes in density-independent mortality rates often lead to abrupt transitions in mean population sizes, and increases in the mortality rate of one predator may decrease the population size of the competing predator. Similarly, increases in the immigration rate of one predator may decrease its own density and increase the density of the other predator. Proportional changes in one predator's birth and death rate functions can have significant effects on the dynamics and mean densities of both predator species. All of these responses to environmental change differ from those observed when competitors coexist stably as the result of resource (prey) partitioning. The patterns described here occur in many other competition models in which there are cycles and differences in the linearity of the responses of consumers to their resources.     

Effects of predation environment and food availability on somatic growth in the Livebearing Fish Brachyrhaphis rhabdophora (Pisces: Poeciliidae)

Variation in somatic growth rates is of great interest to biologists because of the relationship between growth and other fitness‐determining traits, and it results from both genetic and environmentally induced variation (i.e. plasticity). Theoretical predictions suggest that mean somatic growth rates and the shape of the reaction norm for growth can be influenced by variation in predator‐induced mortality rates. Few studies have focused on variation in reaction norms for growth in response to resource availability between high‐predation and low‐predation environments. We used juvenile Brachyrhaphis rhabdophora from high‐predation and low‐predation environments to test for variation in mean growth rates and for variation in reaction norms for growth at two levels of food availability in a common‐environment experiment. To test for variation in growth rates in the field, we compared somatic growth rates in juveniles in high‐predation and low‐predation environments. In the common‐environment experiment, mean growth rates did not differ between fish from differing predation environments, but the interaction between predation environment and food level took the form of a crossing reaction norm for both growth in length and mass. Fish from low‐predation environments exhibited no significant difference in growth rate between high and low food treatments. In contrast, fish from high‐predation environments exhibited variation in growth rates between high and low food treatments, with higher food availability resulting in higher growth rates. In the field, individuals in the high‐predation environment grow at a faster rate than those in low‐predation environments at the smallest sizes (comparable to sizes in the common‐environment experiment). These data provide no evidence for evolved differences in mean growth rates between predation environments. However, fish from high‐predation environments exhibited greater plasticity in growth rates in response to resource availability suggesting that predation environments may exhibit increased variation in food availability for prey fish and consequent selection for plasticity.     

Prey persistence and abundance in systems with intraguild predation and type-2 functional responses

The apparent prevalence of intraguild predation in productive environments has been regarded as puzzling because some simple models suggest that the intraguild prey species is often either reduced in abundance or driven extinct at high resource productivity. While various theoretical mechanisms that avoid this prediction have been uncovered, they have often been viewed as being narrowly applicable. This article examines the fate of the intraguild prey in models in which consumer species may have type-2 functional responses; these are usually characterized by sustained fluctuations in population density at high enough resource productivities. The models also include adaptive, but imperfect diet choice by the top predator. We concentrate on two situations: (1) the prey exhibits less saturation in its functional response to the resource than does the predator and (2) the predator is unable to persist on the basal resource alone. The reasons given by previous studies for discounting these cases are re-examined. The present analysis shows that prey abundance often increases with increasing productivity in both cases, as does the range of prey parameters that allows prey persistence. It is also possible for the prey to coexist with the predator in spite of having a larger equilibrium requirement for the resource. Different assumptions about the dynamics of diet choice can have a large impact on population responses to enrichment. We argue that the persistence and/or increase in abundance of intraguild prey at higher productivity should not be regarded as puzzling because observations are consistent with a range of theoretical models that reflect commonly observed mechanisms.     

Piscivore efficiency and refuging prey: the importance of predator search mode

In predator-prey interactions, the efficiency of the predator is dependent on characteristics of both the predator and the prey, as well as the structure of the environment. In a field enclosure experiment, we tested the effects of a prey refuge on predator search mode, predator efficiency and prey behaviour. Replicated enclosures containing young of the year (0+) and 1-year-old (1+) perch were stocked with 3 differentially sized individuals of either of 2 piscivorous species, perch (Perca fluviatilis), pike (Esox lucius) or no piscivorous predators. Each enclosure contained an open predator area with three small vegetation patches, and a vegetated absolute refuge for the prey. We quantified the behaviour of the predators and the prey simultaneously, and at the end of the experiment the growth of the predators and the mortality and habitat use of the prey were estimated. The activity mode of both predator species was stationary. Perch stayed in pairs in the vegetation patches whereas pike remained solitary and occupied the corners of the enclosure. The largest pike individuals stayed closest to the prey refuge whereas the smallest individuals stayed farthest away from the prey refuge, indicating size-dependent interference among pike. Both size classes of prey showed stronger behavioural responses to pike than to perch with respect to refuge use, distance from refuge and distance to the nearest predator. Prey mortality was higher in the presence of pike than in the presence of perch. Predators decreased in body mass in all treatments, and perch showed a relatively stronger decrease in body mass than pike during the experiment. Growth differences of perch and pike, and mortality differences of prey caused by predation, can be explained by predator morphology, predator attack efficiency and social versus interference behaviour of the predators. These considerations suggest that pike are more efficient piscivores around prey refuges such as the littoral zones of lakes, whereas perch have previously been observed to be more efficient in open areas, such as in the pelagic zones of lakes.     

Environmental fluctuations restrict eco-evolutionary dynamics in predator–prey system

Environmental fluctuations, species interactions and rapid evolution are all predicted to affect community structure and their temporal dynamics. Although the effects of the abiotic environment and prey evolution on ecological community dynamics have been studied separately, these factors can also have interactive effects. Here we used bacteria–ciliate microcosm experiments to test for eco-evolutionary dynamics in fluctuating environments. Specifically, we followed population dynamics and a prey defence trait over time when populations were exposed to regular changes of bottom-up or top-down stressors, or combinations of these. We found that the rate of evolution of a defence trait was significantly lower in fluctuating compared with stable environments, and that the defence trait evolved to lower levels when two environmental stressors changed recurrently. The latter suggests that top-down and bottom-up changes can have additive effects constraining evolutionary response within populations. The differences in evolutionary trajectories are explained by fluctuations in population sizes of the prey and the predator, which continuously alter the supply of mutations in the prey and strength of selection through predation. Thus, it may be necessary to adopt an eco-evolutionary perspective on studies concerning the evolution of traits mediating species interactions.