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.     

Comparing the effects of rapid evolution and phenotypic plasticity on predator-prey dynamics

Ecologists have increasingly focused on how rapid adaptive trait changes can affect population dynamics. Rapid adaptation can result from either rapid evolution or phenotypic plasticity, but their effects on population dynamics are seldom compared directly. Here we examine theoretically the effects of rapid evolution and phenotypic plasticity of antipredatory defense on predator-prey dynamics. Our analyses reveal that phenotypic plasticity tends to stabilize population dynamics more strongly than rapid evolution. It is therefore important to know the mechanism by which phenotypic variation is generated for predicting the dynamics of rapidly adapting populations. We next examine an advantage of a phenotypically plastic prey genotype over the polymorphism of specialist prey genotypes. Numerical analyses reveal that the plastic genotype, if there is a small cost for maintaining it, cannot coexist with the pairs of specialist counterparts unless the system has a limit cycle. Furthermore, for the plastic genotype to replace specialist genotypes, a forced environmental fluctuation is critical in a broad parameter range. When these results are combined, the plastic genotype enjoys an advantage with population oscillations, but plasticity tends to lose its advantage by stabilizing the oscillations. This dilemma leads to an interesting intermittent limit cycle with the changing frequency of phenotypic plasticity.     

Rapid contemporary evolution and clonal food web dynamics

Character evolution that affects ecological community interactions often occurs contemporaneously with temporal changes in population size, potentially altering the very nature of those dynamics. Such eco-evolutionary processes may be most readily explored in systems with short generations and simple genetics. Asexual and cyclically parthenogenetic organisms such as microalgae, cladocerans and rotifers, which frequently dominate freshwater plankton communities, meet these requirements. Multiple clonal lines can coexist within each species over extended periods, until either fixation occurs or a sexual phase reshuffles the genetic material. When clones differ in traits affecting interspecific interactions, within-species clonal dynamics can have major effects on the population dynamics. We first consider a simple predator–prey system with two prey genotypes, parametrized with data from a well-studied experimental system, and explore how the extent of differences in defence against predation within the prey population determine dynamic stability versus instability of the system. We then explore how increased potential for evolution affects the community dynamics in a more general community model with multiple predator and multiple prey genotypes. These examples illustrate how microevolutionary ‘details’ that enhance or limit the potential for heritable phenotypic change can have significant effects on contemporaneous community-level dynamics and the persistence and coexistence of species.     

Measuring the contribution of evolution to community trait structure in freshwater zooplankton

There are currently few predictions about when evolutionary processes are likely to play an important role in structuring community features. Determining predictors that indicate when evolution is expected to impact ecological processes in natural landscapes can help researchers identify eco-evolutionary ‘hotspots', where eco-evolutionary interactions are more likely to occur. Using data collected from a survey in freshwater cladoceran communities, landscape population genetic data and phenotypic trait data measured in a common garden, we applied a Bayesian linear model to assess whether the impact of local trait evolution in the keystone species Daphnia magna on cladoceran community trait values could be predicted by population genetic properties (within-population genetic diversity, genetic distance among populations), ecological properties (Simpson's diversity, phenotypic divergence) or environmental divergence. We found that the impact of local trait evolution varied among communities. Moreover, community diversity and phenotypic divergence were found to be better predictors of the contribution of evolution to community trait values than environmental features or genetic properties of the evolving species. Our results thus indicate the importance of ecological context for the impact of evolution on community features. Our study also demonstrates one way to detect signatures of eco-evolutionary interactions in communities inhabiting heterogeneous landscapes using survey data of contemporary ecological and evolutionary structure.     

Adaptive genetic variation mediates bottom-up and top-down control in an aquatic ecosystem

Research in eco-evolutionary dynamics and community genetics has demonstrated that variation within a species can have strong impacts on associated communities and ecosystem processes. Yet, these studies have centred around individual focal species and at single trophic levels, ignoring the role of phenotypic variation in multiple taxa within an ecosystem. Given the ubiquitous nature of local adaptation, and thus intraspecific variation, we sought to understand how combinations of intraspecific variation in multiple species within an ecosystem impacts its ecology. Using two species that co-occur and demonstrate adaptation to their natal environments, black cottonwood (Populus trichocarpa) and three-spined stickleback (Gasterosteus aculeatus), we investigated the effects of intraspecific phenotypic variation on both top-down and bottom-up forces using a large-scale aquatic mesocosm experiment. Black cottonwood genotypes exhibit genetic variation in their productivity and consequently their leaf litter subsidies to the aquatic system, which mediates the strength of top-down effects from stickleback on prey abundances. Abundances of four common invertebrate prey species and available phosphorous, the most critically limiting nutrient in freshwater systems, are dictated by the interaction between genetic variation in cottonwood productivity and stickleback morphology. These interactive effects fit with ecological theory on the relationship between productivity and top-down control and are comparable in strength to the effects of predator addition. Our results illustrate that intraspecific variation, which can evolve rapidly, is an under-appreciated driver of community structure and ecosystem function, demonstrating that a multi-trophic perspective is essential to understanding the role of evolution in structuring ecological patterns.     

The role of phenotypic plasticity in shaping ecological networks

Plasticity-mediated changes in interaction dynamics and structure may scale up and affect the ecological network in which the plastic species are embedded. Despite their potential relevance for understanding the effects of plasticity on ecological communities, these effects have seldom been analysed. We argue here that, by boosting the magnitude of intra-individual phenotypic variation, plasticity may have three possible direct effects on the interactions that the plastic species maintains with other species in the community: may expand the interaction niche, may cause a shift from one interaction niche to another or may even cause the colonization of a new niche. The combined action of these three factors can scale to the community level and eventually expresses itself as a modification in the topology and functionality of the entire ecological network. We propose that this causal pathway can be more widespread than previously thought and may explain how interaction niches evolve quickly in response to rapid changes in environmental conditions. The implication of this idea is not solely eco-evolutionary but may also help to understand how ecological interactions rewire and evolve in response to global change.     

Floral plasticity: Herbivore‐species‐specific‐induced changes in flower traits with contrasting effects on pollinator visitation

Plant phenotypic plasticity in response to antagonists can affect other community members such as mutualists, conferring potential ecological costs associated with inducible plant defence. For flowering plants, induction of defences to deal with herbivores can lead to disruption of plant–pollinator interactions. Current knowledge on the full extent of herbivore‐induced changes in flower traits is limited, and we know little about specificity of induction of flower traits and specificity of effect on flower visitors. We exposed flowering Brassica nigra plants to six insect herbivore species and recorded changes in flower traits (flower abundance, morphology, colour, volatile emission, nectar quantity, and pollen quantity and size) and the behaviour of two pollinating insects. Our results show that herbivory can affect multiple flower traits and pollinator behaviour. Most plastic floral traits were flower morphology, colour, the composition of the volatile blend, and nectar production. Herbivore‐induced changes in flower traits resulted in positive, negative, or neutral effects on pollinator behaviour. Effects on flower traits and pollinator behaviour were herbivore species‐specific. Flowers show extensive plasticity in response to antagonist herbivores, with contrasting effects on mutualist pollinators. Antagonists can potentially act as agents of selection on flower traits and plant reproduction via plant‐mediated interactions with mutualists.     

Virus mediated trophic interactions between aphids and their natural enemies

Microbial endosymbionts alter the phenotype of their host which may have cascading effects at both population and community levels. However, we currently lack information on whether the effects of viruses on both host phenotypic traits and host population demography can modify interactions with upper trophic levels. To fill this gap, we investigated whether a prevalent densovirus infecting the aphid Myzus persicae (i.e. MpDNV) can modify trophic interactions between host aphids and their natural enemies (i.e. predators and parasitoids) by influencing aphid phenotypic traits (i.e. body mass and defensive behaviours), population demography (i.e. density and age-structure) and susceptibility towards both predation and parasitism. We found that the virus decreased aphid body mass but did not influence their behavioural defences. At the population level, the virus had a minor effect on aphid adult mortality whereas it strongly reduced the density of nymphs and influenced the stage structure of aphid populations. In addition, the virus enhanced the susceptibility of aphids to parasitism regardless of the parasitoid species. Predation rate on adult aphids was not influenced by the virus but ladybeetle predators strongly decreased the number of aphid nymphs, especially for uninfected ones compared to infected ones. As a result, the virus decreased predator effect on aphid populations. By reducing both aphid quality and availability, increasing their susceptibility to parasitism, and modulating predator effect on aphid populations, we highlighted that viral endosymbionts can be prevalent drivers of their host ecology as they modify their phenotypes and interspecific interactions. These virus-mediated ecological effects may have consequences on enemies foraging strategies as well as trophic webs dynamics and structure.     

A history of phenotypic plasticity accelerates adaptation to a new environment

Can a history of phenotypic plasticity increase the rate of adaptation to a new environment? Theory suggests it can be through two different mechanisms. Phenotypically plastic organisms can adapt rapidly to new environments through genetic assimilation, or the fluctuating environments that result in phenotypic plasticity can produce evolvable genetic architectures. In this article, I studied a model of a gene regulatory network that determined a phenotypic character in one population selected for phenotypic plasticity and a second population in a constant environment. A history of phenotypic plasticity increased the rate of adaptation in a new environment, but the amount of this increase was dependent on the strength of selection in the original environment. Phenotypic variance in the original environment predicted the adaptive capacity of the trait within, but not between, plastic and nonplastic populations. These results have implications for invasive species and ecological studies of rapid adaptation.     

Inducible defences and the paradox of enrichment

In order to evaluate the effects of inducible defences on community stability and persistence, we analyzed models of bitrophic and tritrophic food chains that incorporate consumer-induced polymorphisms. These models predict that intra-specific heterogeneity in defence levels resolves the paradox of enrichment for a range of top-down effects that affect consumer death rates and for all possible levels of primary productivity. We show analytically that this stability can be understood in terms of differences in handling times on the different prey types. Our predictions still hold when defences also affect consumer attack rates. The predicted stability occurs in both bitrophic and tritrophic food chains.
Inducible defences may promote population persistence in tritrophic food chains. Here the minimum densities of cycling populations remain bound away from zero, thus decreasing the risk of population extinctions. However, the reverse can be true for the equivalent bitrophic predator–prey model. This shows that theoretical extrapolations from simple to complex communities should be made with caution. Our results show that inducible defences are among the ecological factors that promote stability in multitrophic communities.     

Intraspecific competitive interactions rapidly evolve via spontaneous mutations

Using a mechanistic spatially explicit trait-based neighborhood-model, we quantify the impact of mutations on intraspecific spatial interactions to better understand mechanisms underlying the maintenance of genetic variation and the potential effects of these evolved interactions on the population dynamics of Arabidopsis thaliana. We use 100 twenty-fifth generation mutation accumulation (MA) lines (genotypes) derived from one founder genotype to study mutational effects on neighbor responses in a field experiment. We created individual-based maps (15,000 individuals), including phenotypic variation, to quantify mutational effects within genotypes versus between genotypes on reproduction and survival. At small-scale (within 80 cm of the focal plant), survival is enhanced but seed-set is decreased when a genotype is surrounded by different genotypes. At large-scale (within 200 cm of the focal plant), seed set is facilitated by different genotypes while the same genotype has either no effect or negative effects. The direction of the interactions among MA lines suggests that at small scale these interactions may contribute to the maintenance of genetic variation and at large scale contribute to the survival of the population. This may suggest, that, mutations potentially have immediate effects on population and community dynamics by influencing the outcome of competitive and faciliatory interactions among conspecifics.

     

Linking herbivore-induced defences to population dynamics

1. Theoretical studies have shown that inducible defences have the potential to affect population stability and persistence in bi‐ and tritrophic food chains. Experimental studies on such effects of prey defence strategies on the dynamics of predator–prey systems are still rare. We performed replicated population dynamics experiments using the herbivorous rotifer Brachionus calyciflorus and four strains of closely related algae that show different defence responses to this herbivore. 2. We observed herbivore populations to fluctuate at a higher frequency when feeding on small undefended algae. During these fluctuations minimum rotifer densities remained sufficiently high to ensure population persistence in all the replicates. The initial growth of rotifer populations in this treatment coincided with a sharp drop in algal density. Such a suppression of algae by herbivores was not observed in the other treatments, where algae were larger due to induced or permanent defences. In these treatments we observed rotifer population densities to first rise and then decline. The herbivore went extinct in all replicates with large permanently defended algae. The frequency of herbivore extinctions was intermediate when algae had inducible defences. 3. A variety of alternative mechanisms could explain differential herbivore persistence in the different defence treatments. Our analysis showed the density and fraction of highly edible algal particles to better explain herbivore persistence and extinctions than total algal density, the fraction of highly inedible food particles or the accumulation of herbivore waste products or autotoxins. 4. We argue that the rotifers require a minimum fraction and density of edible food particles for maintenance and reproduction. We conjecture that induced defences in algae may thus favour larger zooplankton species such as Daphnia spp. that are less sensitive to shifts in their food size spectrum, relative to smaller zooplankton species, such as rotifers and in this way contributes to the structuring of planktonic communities.     

Recent advances in ecological stoichiometry: insights for population and community ecology

Conventional theories of population and community dynamics are based on a single currency such as number of individuals, biomass, carbon or energy. However, organisms are constructed of multiple elements and often require them (in particular carbon, phosphorus and nitrogen) in different ratios than provided by their resources; this mismatch may constrain the net transfer of energy and elements through trophic levels. Ecological stoichiometry, the study of the balance of elements in ecological processes, offers a framework for exploring ecological effects of such constraints. We review recent theoretical and empirical studies that have considered how stoichiometry may affect population and community dynamics. These studies show that stoichiometric constraints can affect several properties of populations (e.g. stability, oscillations, consumer extinction) and communities (e.g. coexistence of competitors, competitive interactions between different guilds). We highlight gaps in general knowledge and focus on areas of population and community ecology where incorporation of stoichiometric constraints may be particularly fruitful, such as studies of demographic bottlenecks, spatial processes, and multi-species interactions. Finally, we suggest promising directions for new research by recommending potential study systems (terrestrial insects, detritivory-based webs, soil communities) to improve our understanding of populations and communities. Our conclusion is that a better integration of stoichiometric principles and other theoretical approaches in ecology may allow for a richer understanding of both population and community structure and dynamics.     

Scaling up phenotypic plasticity with hierarchical population models

Individuals respond to different environments by developing different phenotypes, which is generally seen as a mechanism through which individuals can buffer adverse environmental conditions and increase their fitness. To understand the consequences of phenotypic plasticity it is necessary to study how changing a particular trait of an individual affects either its survival, growth, reproduction or a combination of these demographic vital rates (i.e. fitness components). Integrating vital rate changes due to phenotypic plasticity into models of population dynamics allows detailed study of how phenotypic changes scale up to higher levels of integration and forms an excellent tool to distinguish those plastic trait changes that really matter at the population level. A modeling approach also facilitates studying systems that are even more complex: traits and vital rates often co-vary or trade-off with other traits that may show plastic responses over environmental gradients. Here we review recent developments in the literature on population models that attempt to include phenotypic plasticity with a range of evolutionary assumptions and modeling techniques. We present in detail a model framework in which environmental impacts on population dynamics can be followed analytically through direct and indirect pathways that importantly incorporate phenotypic plasticity, trait-trait and trait-vital rate relationships. We illustrate this framework with two case studies: the population-level consequences of phenotypic responses to nutrient enrichment of plant species occurring in nutrient-poor habitats and of responses to changes in flooding regimes due to climate change. We conclude with exciting prospects for further development of this framework: selection analyses, modeling advances and the inclusion of spatial dynamics by considering dispersal traits as well.     

Plasticity is a locally adapted trait with consequences for ecological dynamics in novel environments

Phenotypic plasticity is predicted to evolve in more variable environments, conferring an advantage on individual lifetime fitness. It is less clear what the potential consequences of that plasticity will have on ecological population dynamics. Here, we use an invertebrate model system to examine the effects of environmental variation (resource availability) on the evolution of phenotypic plasticity in two life history traits—age and size at maturation—in long‐running, experimental density‐dependent environments. Specifically, we then explore the feedback from evolution of life history plasticity to subsequent ecological dynamics in novel conditions. Plasticity in both traits initially declined in all microcosm environments, but then evolved increased plasticity for age‐at‐maturation, significantly so in more environmentally variable environments. We also demonstrate how plasticity affects ecological dynamics by creating founder populations of different plastic phenotypes into new microcosms that had either familiar or novel environments. Populations originating from periodically variable environments that had evolved greatest plasticity had lowest variability in population size when introduced to novel environments than those from constant or random environments. This suggests that while plasticity may be costly it can confer benefits by reducing the likelihood that offspring will experience low survival through competitive bottlenecks in variable environments. In this study, we demonstrate how plasticity evolves in response to environmental variation and can alter population dynamics—demonstrating an eco‐evolutionary feedback loop in a complex animal moderated by plasticity in growth.     

How fast is fast? Eco‐evolutionary dynamics and rates of change in populations and phenotypes

It is increasingly recognized that evolution may occur in ecological time. It is not clear, however, how fast evolution – or phenotypic change more generally – may be in comparison with the associated ecology, or whether systems with fast ecological dynamics generally have relatively fast rates of phenotypic change. We developed a new dataset on standardized rates of change in population size and phenotypic traits for a wide range of species and taxonomic groups. We show that rates of change in phenotypes are generally no more than 2/3, and on average about 1/4, the concurrent rates of change in population size. There was no relationship between rates of population change and rates of phenotypic change across systems. We also found that the variance of both phenotypic and ecological rates increased with the mean across studies following a power law with an exponent of two, while temporal variation in phenotypic rates was lower than in ecological rates. Our results are consistent with the view that ecology and evolution may occur at similar time scales, but clarify that only rarely do populations change as fast in traits as they do in abundance.     

Eco-evolutionary dynamics in Pacific salmon

Increasing acceptance of the idea that evolution can proceed rapidly has generated considerable interest in understanding the consequences of ongoing evolutionary change for populations, communities and ecosystems. The nascent field of 'eco-evolutionary dynamics' considers these interactions, including reciprocal feedbacks between evolution and ecology. Empirical support for eco-evolutionary dynamics has emerged from several model systems, and we here present some possibilities for diverse and strong effects in Pacific salmon (Oncorhynchus spp.). We specifically focus on the consequences that natural selection on body size can have for salmon population dynamics, community (bear-salmon) interactions and ecosystem process (fluxes of salmon biomass between habitats). For example, we find that shifts in body size because of selection can alter fluxes across habitats by up to 11% compared with ecological (that is, numerical) effects. More generally, we show that selection within a generation can have large effects on ecological dynamics and so should be included within a complete eco-evolutionary framework.     

Inducible defences prevent strong population fluctuations in bi- and tritrophic food chains

Recent theoretical work ( Vos et al. 2004 ) predicts that inducible defences prevent strong population fluctuations under high levels of nutrient enrichment. Here we evaluate this model prediction and show that inducible defences in algae stabilize the dynamics of experimentally assembled bi‐ and tritrophic planktonic food chains. At high phosphorus levels, we observed strong population fluctuations in all food chains with undefended algae. These fluctuations did not occur when algae had inducible defences. At low phosphorus levels, we observed deterministic consumer extinctions, as predicted by stoichiometric theory. Our study thus shows that both biotically and abiotically induced changes in algal food quality affect the stability and persistence of planktonic food chains.     

Induced defences alter the strength and direction of natural selection on reproductive traits in common milkweed

Evolutionary biologists have long sought to understand the ecological processes that generate plant reproductive diversity. Recent evidence indicates that constitutive antiherbivore defences can alter natural selection on reproductive traits, but it is unclear whether induced defences will have the same effect and whether reduced foliar damage in defended plants is the cause of this pattern. In a factorial field experiment using common milkweed, Asclepias syriaca L., we induced plant defences using jasmonic acid (JA) and imposed foliar damage using scissors. We found that JA‐induced plants experienced selection for more inflorescences that were smaller in size (fewer flowers), whereas control plants only experienced a trend towards selection for larger inflorescences (more flowers); all effects were independent of foliar damage. Our results demonstrate that induced defences can alter both the strength and direction of selection on reproductive traits, and suggest that antiherbivore defences may promote the evolution of plant reproductive diversity.     

The timescale of environmental fluctuations determines the competitive advantages of phenotypic plasticity and rapid evolution

Organisms can respond to fluctuating environments by phenotypic plasticity and rapid evolution, both occurring on similar timescales to the environmental fluctuations. Because each adaptation mechanism has been independently studied, the effects of different adaptation mechanisms on ecological dynamics are not well understood. Here, using mathematical modeling, we compared the advantages of phenotypic plasticity and rapid evolution under conditions where the environment fluctuated between two states on various timescales. The results indicate that the advantages of phenotypic plasticity under environmental fluctuations on different timescales depend on the cost and the speed of plasticity. Both the speed of plastic adaptation and the cost of plasticity affect competition results, while the quantitative effects of them vary depending on the timescales. When the environment fluctuates on short timescales, the two populations with evolution and plasticity coexist, although the population with evolution is dominant. On moderate timescales, the two populations also coexist; however, the population with plasticity becomes dominant. On long timescales, whether the population with phenotypic plasticity or evolution is more advantageous depended on the cost of plasticity. Moreover, our results indicate that the mechanisms resulting in the dominance of the plastic population over the population with evolution are different depending on the timescales of environmental fluctuations. Therefore, the timescales of environmental fluctuations deserve more attention if we are to better understand the detailed competition results underlying phenotypic variation.