The effects of switching behavior on the evolutionary diversification of generalist consumers

Mathematical models of consumer-resource systems explore the evolution of a morphological trait that determines two resource acquisition rates in a generalist consumer. The consumer also has the ability to adjust its relative consumption of the two resources via behavioral (or developmental) plasticity subject to a trade-off. The analysis examines both stable systems and those with sustained fluctuations in abundance. In both cases, it seeks to determine how the behavioral choice affects the evolution of the morphological characters. The presence of adaptive switching behavior transforms the shape of the relationship between the morphological character and fitness in a manner that usually leads to evolution of two or more morphological types. As in models without switching, the presence of sustained cycles in resource densities often allows the evolution of a generalist as well as two specialists. However, switching expands and shifts the parameter regions yielding this outcome and in some cases allows the evolution and coexistence of at least two generalists as well as the two specialists. This level of diversity supported by only two resources is not seen in the absence of behavioral choice and resource cycles. The results suggest major roles for both behavior and environmental variation in adaptive radiation.     

The evolution and coexistence of generalist and specialist herbivores under between-plant competition

Consumer-resource models have been used extensively to study the evolution and coexistence of generalist and specialist consumers. However, current consumer-resource models do not take into account competition between resources or only incorporate intraspecific competition phenomenologically with, for example, a logistic growth function. Here, we mechanistically incorporate competition in an existing two-resource model, by introducing nutrient-limited resource growth and setting the total amount of nutrients (free or contained in consumers and resources) to a fixed value. In addition to the three combinations of generalists and specialists found in previous models, we find four other evolutionary outcomes, depending on the strength of the consumer trade-off: coexistence of one specialist and a generalist and three types of evolutionary cycling. Furthermore, which outcomes are most likely depends strongly on the combination of intrinsic growth rate of resources and the total amount of nutrients in the system. Our results suggest that the realistic assumption of nutrient competition may shed new light on the evolution of the multitude of strategies in real systems.     

How do generalist consumers coexist over evolutionary time? An explanation with nutrition and tradeoffs

Generalist consumers commonly coexist in many ecosystems. Yet, eco-evolutionary theory poses a problem with this observation: generalist consumers (usually) cannot coexist stably. To provide a solution to this theory-observation dissonance, we analyzed a simple eco-evolutionary consumer resource model. We modeled consumption of two nutritionally interactive resources by species which evolve their resource encounter rates subject to a tradeoff. As shown previously, consumers can ecologically coexist through tradeoffs in resource encounter rates; however, this coexistence is evolutionary unstable. Here, we find that nutritional interactions between resources and the shape of acquisition tradeoffs produce very similar evolutionary outcomes in isolation. Specifically, they produce evolutionarily stable communities composed either of two specialists (concave acquisition tradeoff or antagonistic nutrition) or a single generalist (convex acquisition tradeoff or complementary nutrition). Thus, the generalist-coexistence problem remains. However, the combination of nonlinear resource acquisition tradeoffs with nonlinear resource nutritional relationships creates selection forces that can push and pull against each other. Ultimately, this push-pull dynamic can stabilize the coexistence of two competing generalist consumers—but only when we coupled a convex acquisition tradeoff with antagonistic nutrition. Thus, our model here offers some resolution to the generalist-coexistence problem in eco-evolutionary, consumer-resource theory.     

The evolution of resource specialization through frequency-dependent and frequency-independent mechanisms

Levins's fitness set approach has shaped the intuition of many evolutionary ecologists about resource specialization: if the set of possible phenotypes is convex, a generalist is favored, while either of the two specialists is predicted for concave phenotype sets. An important aspect of Levins's approach is that it explicitly excludes frequency-dependent selection. Frequency dependence emerged in a series of models that studied the degree of character displacement of two consumers coexisting on two resources. Surprisingly, the evolutionary dynamics of a single consumer type under frequency dependence has not been studied in detail. We analyze a model of one evolving consumer feeding on two resources and show that, depending on the trait considered to be subject to evolutionary change, selection is either frequency independent or frequency dependent. This difference is explained by the effects different foraging traits have on the consumer-resource interactions. If selection is frequency dependent, then the population can become dimorphic through evolutionary branching at the trait value of the generalist. Those traits with frequency-independent selection, however, do indeed follow the predictions based on Levins's fitness set approach. This dichotomy in the evolutionary dynamics of traits involved in the same foraging process was not previously recognized.     

The prerequisites for and likelihood of generalist-specialist coexistence

Mathematical models of three-consumer-two-resource systems are used to explore the possibility of coexistence when one consumer is a generalist utilizing both resources, and the other two are specialists utilizing only one. Such coexistence requires strongly saturating functional or numerical responses in at least one consumer and the presence of sustained asynchronous variation in resource abundances. Given these conditions, the effects of three dichotomous factors on the range of parameters allowing coexistence are examined: flexible versus inflexible resource choice by the generalist, endogenous or exogenous cause of resource cycles, and location of the two resources in a single habitat versus two habitats. Coexistence of all three species is found to be possible for all combinations of these factors except for inflexible choice in a two-habitat environment. Generalists experience frequency-dependent fitness because, when they are abundant, they synchronize resource cycles and/or reduce their amplitude. When the generalist can adaptively adjust its relative foraging on the two resources, coexistence conditions are broadened considerably, and coexistence commonly occurs readily with exogenous variation in resource growth and with resources located in distinct habitats. Adaptive behavior increases the generalist's ability to both synchronize and dampen resource cycles.     

Resource-dependent reproductive adjustment and the stability of consumer-resource dynamics

This study explored a consumer-resource model including reproductive and nonreproductive subpopulations of the consumer to consider whether resource-dependent reproductive adjustment by the consumer would stabilize consumer-resource dynamics. The model assumed that decreasing (increasing) resource availability caused reproductive suppression (facilitation), and that the reproductive consumer had a higher mortality rate than the nonreproductive one (i.e., a trade-off between reproduction and survival). The model predicted that the variability would be reduced when the consumer had a strong tendency to suppress reproduction in response to low resource availability or when the cost of reproduction was high, although consumer extinction became more likely. Furthermore, when the consumer-resource dynamics converged to limit cycles, reproductive adjustment enhanced the long-term average of the consumer density. It was also predicted that if reproductive suppression enhanced resource consumption efficiency (i.e., a trade-off between reproduction and foraging), then it would destabilize the system by canceling the stabilizing effect of the reproductive adjustment itself. These results suggest that it is necessary not only to identify the costs of reproduction, but also to quantify the changes in individual-level performances due to reproduction in order to understand the ecological consequences of reproductive adjustment.     

On the evolution of specialization with a mechanistic underpinning in structured metapopulations

We analyze the evolution of specialization in resource utilization in a discrete-time metapopulation model using the adaptive dynamics approach. The local dynamics in the metapopulation are based on the Beverton-Holt model with mechanistic underpinnings. The consumer faces a trade-off in the abilities to consume two resources that are spatially heterogeneously distributed to patches that are prone to local catastrophes. We explore the factors favoring the spread of generalist or specialist strategies. Increasing fecundity or decreasing catastrophe probability favors the spread of the generalist strategy and increasing environmental heterogeneity enlarges the parameter domain where the evolutionary branching is possible. When there are no catastrophes, increasing emigration diminishes the parameter domain where the evolutionary branching may occur. Otherwise, the effect of emigration on evolutionary dynamics is non-monotonous: both small and large values of emigration probability favor the spread of the specialist strategies whereas the parameter domain where evolutionary branching may occur is largest when the emigration probability has intermediate values. We compare how different forms of spatial heterogeneity and different models of local growth affect the evolutionary dynamics. We show that even small changes in the resource dynamics may have outstanding evolutionary effects to the consumers.     

Host specialist clownfishes are environmental niche generalists

Why generalist and specialist species coexist in nature is a question that has interested evolutionary biologists for a long time. While the coexistence of specialists and generalists exploiting resources on a single ecological dimension has been theoretically and empirically explored, biological systems with multiple resource dimensions (e.g. trophic, ecological) are less well understood. Yet, such systems may provide an alternative to the classical theory of stable evolutionary coexistence of generalist and specialist species on a single resource dimension. We explore such systems and the potential trade-offs between different resource dimensions in clownfishes. All species of this iconic clade are obligate mutualists with sea anemones yet show interspecific variation in anemone host specificity. Moreover, clownfishes developed variable environmental specialization across their distribution. In this study, we test for the existence of a relationship between host-specificity (number of anemones associated with a clownfish species) and environmental-specificity (expressed as the size of the ecological niche breadth across climatic gradients). We find a negative correlation between host range and environmental specificities in temperature, salinity and pH, probably indicating a trade-off between both types of specialization forcing species to specialize only in a single direction. Trade-offs in a multi-dimensional resource space could be a novel way of explaining the coexistence of generalist and specialists.     

Decreasing functional responses as a result of adaptive consumer behavior

Summary Several different mechanisms that may produce decreasing functional responses are investigated using models that assume that an optimally foraging consumer is exploiting one or two resources. Decreasing functional responses are associated with situations in which there are costs to resource consumption. If the process of resource acquisition has costs, decreasing functional responses may occur when there is a single homogeneous resource. If the cost is solely a function of the amount of resource ingested, decreasing functional responses on a single resource do not occur. Both types of cost can produce decreasing functional responses when there are two resource types and a trade-off relationship between consumption of one and consumption of the other. Decreasing functional responses seem to be most likely to occur on a food that yields high benefits and costs per unit of foraging time or effort when there is an alternative resource which yields low benefits and costs. Given this type of foraging choice, the functional response is most likely to decrease when the benefits of ingestion increase at a decreasing rate, and the costs of ingestion increase at an increasing rate with amount ingested. An important and unique consequence of decreasing functional responses is the possibility of population cycles in differential equation models of consumer-resource systems with non-reproducing resources; this is illustrated with a simple comsumer-resource model.     

The Evolution of Resource Adaptation: How Generalist and Specialist Consumers Evolve

Why and how specialist and generalist strategies evolve are important questions in evolutionary ecology. In this paper, with the method of adaptive dynamics and evolutionary branching, we identify conditions that select for specialist and generalist strategies. Generally, generalist strategies evolve if there is a switching benefit; specialists evolve if there is a switching cost. If the switching cost is large, specialists always evolve. If the switching cost is small, even though the consumer will first evolve toward a generalist strategy, it will eventually branch into two specialists.     

The interplay between behavior and morphology in the evolutionary dynamics of resource specialization

We analyze the consequences of diet choice behavior for the evolutionary dynamics of foraging traits by means of a mathematical model. The model is characterized by the following features. Consumers feed on two different substitutable resources that are distributed in a fine-grained manner. On encounter with a resource item, consumers decide whether to attack it so as to maximize their energy intake. Simultaneously, evolutionary change occurs in morphological traits involved in the foraging process. The assumption here is that evolution is constrained by a trade-off in the consumer's ability to forage on the alternative resources. The model predicts that flexible diet choice behavior can guide the direction of evolutionary change and mediate coexistence of different consumer types. Such polymorphisms can evolve from a monomorphic population at evolutionary branching points and also at points where a small genetic change in a trait can provoke a sharp instantaneous and nongenetic change in choice behavior. In the case of weak trade-offs, the evolutionary dynamics of a dimorphic consumer population can lead to alternative evolutionarily stable communities. The robustness of these predictions is checked with individual-based simulations and by relaxing the assumption of optimally foraging consumers.     

High competition with low similarity and low competition with high similarity: exploitative and apparent competition in consumer-resource systems

This article investigates the relationship between the similarity of resource capture abilities and the amount of competition between two consumer species that exploit common resources. Most of the analysis is based on a consumer-resource model introduced by Robert MacArthur. Contrary to many statements in the literature and in textbooks, measures of competition may decrease as similarity increases and may be greatest when similarity of the two species' sets of resource capture rates is very low. High competition with low similarity may occur whether competition is measured by a competition coefficient near equilibrium or is measured by the proportional increase in a species' population density when its competitor is removed. However, these two measures may differ considerably and may change in opposite directions with a given change in similarity. The general conditions required for such counterintuitive relationships between similarity and competition are that the consumer species have relatively low resource requirements for successful reproduction and that the resources be self-reproducing. These same conditions also frequently lead to exclusion of one or more resources via apparent competition, and this is always true of MacArthur's model. A variety of other models of competition are analyzed, and circumstances most likely to produce large competitive effects with little overlap are identified.     

Evolutionary branching and evolutionarily stable coexistence of predator species: Critical function analysis

On the ecological timescale, two predator species with linear functional responses can stably coexist on two competing prey species. In this paper, with the methods of adaptive dynamics and critical function analysis, we investigate under what conditions such a coexistence is also evolutionarily stable, and whether the two predator species may evolve from a single ancestor via evolutionary branching. We assume that predator strategies differ in capture rates and a predator with a high capture rate for one prey has a low capture rate for the other and vice versa. First, by using the method of critical function analysis, we identify the general properties of trade-off functions that allow for evolutionary branching in the predator strategy. It is found that if the trade-off curve is weakly convex in the vicinity of the singular strategy and the interspecific prey competition is not strong, then this singular strategy is an evolutionary branching point, near which the resident and mutant predator populations can coexist and diverge in their strategies. Second, we find that after branching has occurred in the predator phenotype, if the trade-off curve is globally convex, the predator population will eventually branch into two extreme specialists, each completely specializing on a particular prey species. However, in the case of smoothed step function-like trade-off, an interior dimorphic singular coalition becomes possible, the predator population will eventually evolve into two generalist species, each feeding on both of the two prey species. The algebraical analysis reveals that an evolutionarily stable dimorphism will always be attractive and that no further branching is possible under this model.     

THE ECO‐EVOLUTIONARY RESPONSES OF A GENERALIST CONSUMER TO RESOURCE COMPETITION

This article explores the combined evolutionary and ecological responses of resource uptake abilities in a generalist consumer to exploitative competition for one resource using a simple 2‐resource model. It compares the sizes of ecologically and evolutionarily caused changes in population densities in cases where the original consumer has a strong or a weak trade‐off in its abilities to consume the two resources. The analysis also compares the responses of the original species to competition when the competitor's population size is or is not limited by the shared resource. Although divergence in resource use traits in the resident generalist consumer is expected under all scenarios when resources are substitutable, the changes in population densities of the resources and resident consumer frequently differ between scenarios. The population of the original consumer often decreases as a result of its own adaptive divergence, and this decrease is often much greater than the initial ecological decrease. If the evolving consumer has a strong trade‐off, the overlapped resource increases in equilibrium population density in response to being consumed by a generalist competitor. Some of these predictions differ qualitatively in alternative scenarios involving sustained variation in population densities or nutritionally essential resources.     

Natural enemy specialization and the period of population cycles

The dynamical consequences of multiple‐species interactions remain an elusive and fiercely debated topic. Recently, Murdoch and colleagues proposed a general rule for the dynamics of generalist natural enemies: when periodic, they exhibit single generation cycles (SGCs), similar to single species systems. This contrasts markedly with specialists, which tend to show classic (longer period) consumer–resource cycles. Using a well‐studied laboratory system, we show that this general rule is contradicted when we consider resource age‐structure.     

A newly discovered role of evolution in previously published consumer–resource dynamics

Consumer–resource interactions are fundamental components of ecological communities. Classic features of consumer–resource models are that temporal dynamics are often cyclic, with a ¼‐period lag between resource and consumer population peaks. However, there are few published empirical examples of this pattern. Here, we show that many published examples of consumer–resource cycling show instead patterns indicating eco‐evolutionary dynamics. When prey evolve along a trade‐off between defence and competitive ability, two‐species consumer–resource cycles become longer and antiphase (half‐period lag, so consumer maxima coincide with minima of the resource species). Using stringent criteria, we identified 21 two‐species consumer–resource time series, published between 1934 and 1997, suitable to investigate for eco‐evolutionary dynamics. We developed a statistical method to probe for a transition from classic to eco‐evolutionary cycles, and find evidence for eco‐evolutionary type cycles in about half of the studies. We show that rapid prey evolution is the most likely explanation for the observed patterns.     

Dispersal and the evolution of specialisation in a two-habitat type metapopulation

Metapopulation theory for the evolution of specialisation is virtually absent. In this article, therefore, we study a metapopulation model for consumers with a fitness trade-off between two habitats. We focus on effects of habitat abundance, dispersal rate and trade-off strength on the evolution of specialisation under two types of trade-off. Adaptation affects either the intrinsic growth rates r or the carrying capacities K. Depending on dispersal rate and trade-off strength, evolution can result in one generalist, one specialist or two specialist types. Higher dispersal rate and a weaker trade-off favour the evolution of a generalist, for both trade-off structures. However, we also find differences between the two trade-off structures. Our results are qualitatively similar to analyses of two-patch models, suggesting that insights from such simpler models can be extrapolated to metapopulation models. Additional effects, however, occur because in classical metapopulations patch lifetime depends on extinction rate. Counterintuitively, this favours the evolution of specialisation when the trade-off affects r.     

Evolution of dispersal in a multi‐trophic community context

Much is known about the evolution of dispersal when species interact with their resources or natural enemies, but very little is known about dispersal evolution when species interact with both resources and natural enemies. Here I investigate how the dispersal of an intermediate consumer evolves in response to its interactions with a basal resource and top predator. I find that dispersal evolution is possible even when the consumer species is not directly affected by environmental variability, but rather experiences the consequences that such variability has on its resource and predator. Spatial variation in the consumer's fitness is driven by spatial heterogeneity in resource productivity, which determines whether a predator can colonize a resource‐consumer community. Temporal variation in the consumer's fitness is driven by random disturbances that cause periodic local extinctions of the predator, followed by recolonizations that lead to transient fluctuations in consumer abundance. When spatial variation in resource productivity is low and the predator can colonize all patches in the landscape, there is no spatial variation in consumer fitness but temporal variation in fitness favors the evolution of a dispersal monomorphism. When spatial variation in resource productivity is high and the predator cannot colonize many patches in the landscape, spatial variation in fitness selects against dispersal. In this case, temporal variation can promote the evolution of a dispersal polymorphism with sedentary and mobile phenotypes, but only for certain types of tri‐trophic interactions. This finding underscores the importance of indirect interactions in shaping the evolution of dispersal. While the ecological community can provide a strong selective environment for the evolution of dispersal, the nature of interactions between trophic levels can also impose constraints on evolution.     

Discrete consumers,small scale resource heterogeneity,and population stability

We present a consumer-resource model in which individual consumers subsist on a continuum of resource distributed over a very large number of small “bite-sized” patches, each patch being sufficiently small that all its resource is eaten whenever a consumer visits. This form of consumer–resource interaction forces a heterogeneous distribution of resource among the patches, and may dampen out the large amplitude, consumer-resource cycles that are predicted by traditional models of well-mixed, spatially homogeneous systems. The resource equilibrium does not increase with enrichment, a prediction that distinguishes this model from models that invoke direct or indirect consumer density dependence as a stabilizing mechanism.     

Evolution of specialization in resource utilization in structured metapopulations

We study the evolution of resource utilization in a structured discrete-time metapopulation model with an infinite number of patches, prone to local catastrophes. The consumer faces a trade-off in the abilities to consume two resources available in different amounts in each patch. We analyse how the evolution of specialization in the utilization of the resources is affected by different ecological factors: migration, local growth, local catastrophes, forms of the trade-off and distribution of the resources in the patches. Our modelling approach offers a natural way to include more than two patch types into the models. This has not been usually possible in the previous spatially heterogeneous models focusing on the evolution of specialization.