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.     

Adaptive change in the resource-exploitation traits of a generalist consumer: the evolution and coexistence of generalists and specialists

Mathematical models of consumer-resource systems are used to explore the evolution of traits related to resource acquisition in a generalist consumer species that is capable of exploiting two resources. The analysis focuses on whether evolution of traits determining the capture rates of two resources by a consumer species produce one generalist, two specialists, or all three types, when all types are characterized by a common fitness function. In systems with a stable equilibrium, evolution produces one generalist or two specialists, depending on the second derivative of the trade-off relationship. When there are sustained population fluctuations, the nature of the trade-off between the consumer's capture rates of the two resources still plays a key role in determining the evolutionary outcome. If the trade-off is described by a choice variable between zero and one that is raised to a power n, polymorphic states are possible when n > 1, which implies a positive second derivative of the curve. These states are either dimorphism, with two relatively specialized consumer types, or trimorphism, with a single generalist type and two specialists. Both endogenously driven consumer-resource cycles, and fluctuations driven by an environmental variable affecting resource growth are considered. Trimorphic evolutionary outcomes are relatively common in the case of endogenous cycles. In contrast to a previous study, these trimorphisms can often evolve even when new lineages are constrained to have phenotypes very similar to existing lineages. Exogenous cycles driven by environmental variation in resource growth rates appear to be much less likely to produce a mixture of generalists and specialists than are endogenous consumer-resource cycles.     

Quantitative descriptions of resource choice in ecological models

This article reviews the subject of resource choice by consumers. It is concerned with how such choice has been and should be represented in quantitative ecological models. This requires consideration of the dynamics of behavioral change and the fitness consequences of different resource intake rates. The topic is important because of the impact of choice on the functional response of the consumer to each of the resources it consumes. A variety of open questions related to choice are addressed. These include: the relationship between optimal diet choice and switching; the relationship between adaptive choice of two or resources and type-3 functional responses to a single resource; whether switching behavior requires choice and whether choice always results in switching behavior; why partial preferences are observed; whether choice between habitats is fundamentally different from choice within habitats; how between-individual variation in parameters related to resource use alters functional responses measured at the population level. The impacts of choice on stability are discussed briefly. The costs of increased resource use and the type of nutritional interactions between resources are particularly important determinants of adaptive resource choice, and are considered in some detail.     

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 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.     

Increased competition as a cost of specialization during the evolution of resource polymorphism

Identifying the factors that promote or preclude the evolution of resource polymorphism is essential for understanding the origins of diversity. Although such polymorphisms have long been viewed as an adaptive response to intraspecific competition, they are by no means ubiquitous, even in populations experiencing strong competition. In the present study, we examined a potentially important cost of resource polymorphism. Specifically, resource polymorphism typically entails the evolution of one or more resource‐use specialists, and these specialists may suffer more from competition with other specialists than generalists would with other generalists. Using spadefoot toad tadpoles as a model system, we combined stable isotope analyses with an experiment aiming to characterize dietary differences between alternative carnivore and omnivore morphs and to assess the potential ecological consequences of any such differences. We found that carnivores and omnivores represent alternative trophic specialists and generalists, respectively. We also established that the specialist morph (carnivores) experienced greater intramorph competition than the generalist morph (omnivores). We hypothesize that the greater intramorph competition faced by specialists stems ultimately from functional limitations associated with trophic specialization, which prevent specialists from switching to alternative resources when their resource is depleted. These costs may even preclude the evolution of distinct resource‐use specialists, and hence resource polymorphism, in certain populations. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ??, ??–??.     

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.     

Dynamic versus instantaneous models of diet choice

We investigate the dynamics of a series of two-prey-one-predator models in which the predator exhibits adaptive diet choice based on the different energy contents and/or handling times of the two prey species. The predator is efficient at exploiting its prey and has a saturating functional response; these two features combine to produce sustained population cycles over a wide range of parameter values. Two types of models of behavioral change are compared. In one class of models ("instantaneous choice"), the probability of acceptance of the poorer prey by the predator instantaneously approximates the optimal choice, given current prey densities. In the second class of models ("dynamic choice"), the probability of acceptance of the poorer prey is a dynamic variable, which begins to change in an adaptive direction when prey densities change but which requires a finite amount of time to approach the new optimal behavior. The two types of models frequently predict qualitatively different population dynamics of the three-species system, with chaotic dynamics and complex cycles being a common outcome only in the dynamic choice models. In dynamic choice models, factors that reduce the rate of behavioral change when the probability of accepting the poorer prey approaches extreme values often produce complex population dynamics. Instantaneous and dynamic models often predict different average population densities and different indirect interactions between prey species. Alternative dynamic models of behavior are analyzed and suggest, first, that instantaneous choice models may be good approximations in some circumstances and, second, that different types of dynamic choice models often lead to significantly different population dynamics. The results suggest possible behavioral mechanisms leading to complex population dynamics and highlight the need for more empirical study of the dynamics of behavioral change.     

The effect of the Holling type II functional response on apparent competition

This article analyzes the classical 2-resource-1-consumer apparent competition community module with the Holling type II functional response. Two types of resource regulation (top-down vs. combined top-down and bottom-up) and two types of consumer behaviors (inflexible consumers with fixed preferences for resources vs. adaptive consumers) are considered. When resources grow exponentially and consumers are inflexible foragers, one resource is always outcompeted due to strong apparent competition. Density dependent resource growth relaxes apparent competition so that resources can coexist. As multiple attractors (either equilibria or limit cycles) coexist, population dynamics and community composition depend on initial population densities. Population dynamics change dramatically when consumers forage adaptively. In this case, the results both for top-down, and combined top-down and bottom-up regulation are similar and they show that species persistence occurs for a much larger set of parameter values when compared with inflexible consumers. Moreover, population dynamics will be chaotic when resource carrying capacities are high enough. This shows that adaptive consumer switching can destabilize population dynamics.     

Coexistence and community structure in a consumer resource model with implicit stoichiometry

We combine stoichiometry theory and optimal foraging theory into the MacArthur consumer-resource model. This generates predictions for diet choice, coexistence, and community structure of heterotroph communities. Tradeoffs in consumer resource-garnering traits influence community outcomes. With scarce resources, consumers forage opportunistically for complementary resources and may coexist via tradeoffs in resource encounter rates. In contrast to single currency models, stoichiometry permits multiple equilibria. These alternative stable states occur when tradeoffs in resource encounter rates are stronger than tradeoffs in elemental conversion efficiencies. With abundant resources consumers exhibit partially selective diets for essential resources and may coexist via tradeoffs in elemental conversion efficiencies. These results differ from single currency models, where adaptive diet selection is either opportunistic or selective. Interestingly, communities composed of efficient consumers share many of the same properties as communities based on substitutable resources. However, communities composed of relatively inefficient consumers behave similarly to plant communities as characterized by Tilman’s consumer resource theory. The results of our model indicate that the effects of stoichiometry theory on community ecology are dependent upon both consumer foraging behavior and the nature of resource garnering tradeoffs.     

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.     

Foraging performance of diet-induced morphotypes in pumpkinseed sunfish (Lepomis gibbosus) favours resource polymorphism

Morphological plasticity can influence adaptive divergence when it affects fitness components such as foraging performance. We induced morphological variation in pumpkinseed sunfish (Lepomis gibbosus) ecomorphs and tested for effects on foraging performance. Young-of-year pumpkinseed sunfish from littoral and pelagic lake habitats were reared each on a 'specialist diet' representing their native habitat-specific prey, or a 'generalist diet' reflecting a combination of native and non-native prey. Specialist and generalist diets, respectively, induced divergent and intermediate body forms. Specialists had the highest capture success on their native prey whereas generalist forms were inferior. Specialists faced trade-offs across prey types. However, pelagic specialists also had the highest intake rate on both prey types suggesting that foraging trade-offs are relaxed when prey are abundant. This increases the likelihood of a resource polymorphism because the specialized pelagic form can be favoured by directional selection when prey are abundant and by diversifying selection when prey resources are restricted.     

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.     

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.     

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.     

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.     

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.     

Evolution of resource specialisation in competitive metacommunities

Spatial environmental heterogeneity coupled with dispersal can promote ecological persistence of diverse metacommunities. Does this premise hold when metacommunities evolve? Using a two‐resource competition model, we studied the evolution of resource‐uptake specialisation as a function of resource type (substitutable to essential) and shape of the trade‐off between resource uptake affinities (generalist‐ to specialist‐favouring). In spatially homogeneous environments, evolutionarily stable coexistence of consumers is only possible for sufficiently substitutable resources and specialist‐favouring trade‐offs. Remarkably, these same conditions yield comparatively low diversity in heterogeneous environments, because they promote sympatric evolution of two opposite resource specialists that, together, monopolise the two resources everywhere. Consumer diversity is instead maximised for intermediate trade‐offs and clearly substitutable or clearly essential resources, where evolved metacommunities are characterised by contrasting selection regimes. Taken together, our results present new insights into resource‐competition‐mediated evolutionarily stable diversity in homogeneous and heterogeneous environments, which should be applicable to a wide range of systems.     

PREY ADAPTATION AS A CAUSE OF PREDATOR-PREY CYCLES

We analyze simple models of predator-prey systems in which there is adaptive change in a trait of the prey that determines the rate at which it is captured by searching predators. Two models of adaptive change are explored: (1) change within a single reproducing prey population that has genetic variation for vulnerability to capture by the predator; and (2) direct competition between two independently reproducing prey populations that differ in their vulnerability. When an individual predator's consumption increases at a decreasing rate with prey availability, prey adaptation via either of these mechanisms may produce sustained cycles in both species' population densities and in the prey's mean trait value. Sufficiently rapid adaptive change (e.g., behavioral adaptation or evolution of traits with a large additive genetic variance), or sufficiently low predator birth and death rates will produce sustained cycles or chaos, even when the predator-prey dynamics with fixed prey capture rates would have been stable. Adaptive dynamics can also stabilize a system that would exhibit limit cycles if traits were fixed at their equilibrium values. When evolution fails to stabilize inherently unstable population interactions, selection decreases the prey's escape ability, which further destabilizes population dynamics. When the predator has a linear functional response, evolution of prey vulnerability always promotes stability. The relevance of these results to observed predator-prey cycles is discussed.