Adaptive dynamics of competition for nutritionally complementary resources: character convergence, displacement, and parallelism

Consumers acquire essential nutrients by ingesting the tissues of resource species. When these tissues contain essential nutrients in a suboptimal ratio, consumers may benefit from ingesting a mixture of nutritionally complementary resource species. We investigate the joint ecological and evolutionary consequences of competition for complementary resources, using an adaptive dynamics model of two consumers and two resources that differ in their relative content of two essential nutrients. In the absence of competition, a nutritionally balanced diet rarely maximizes fitness because of the dynamic feedbacks between uptake rate and resource density, whereas in sympatry, nutritionally balanced diets maximize fitness because competing consumers with different nutritional requirements tend to equalize the relative abundances of the two resources. Adaptation from allopatric to sympatric fitness optima can generate character convergence, divergence, and parallel shifts, depending not on the degree of diet overlap but on the match between resource nutrient content and consumer nutrient requirements. Contrary to previous verbal arguments that suggest that character convergence leads to neutral stability, coadaptation of competing consumers always leads to stable coexistence. Furthermore, we show that incorporating costs of consuming or excreting excess nonlimiting nutrients selects for nutritionally balanced diets and so promotes character convergence. This article demonstrates that resource-use overlap has little bearing on coexistence when resources are nutritionally complementary, and it highlights the importance of using mathematical models to infer the stability of ecoevolutionary dynamics.     

How does the magnitude of genetic variation affect ecological and reproductive character displacement?

While previous studies on character displacement tended to focus on trait divergence and convergence as a result of long-term evolution, recent studies suggest that character displacement can be a special case of evolutionary rescue, where rapid evolution prevents species extinction by weakening interspecific competition. Here we analyzed a simple model to examine how the magnitude of genetic variation affects evolutionary rescue via ecological and reproductive character displacement that weakens interspecific competition in exploitation of shared resources (i.e., resource competition) and in the mating process caused by incomplete species recognition (i.e., reproductive interference), respectively. We found that slow trait divergence due to small genetic variance results in species extinction in reproductive character displacement but not in ecological character displacement. This is because one species becomes rare in slow character displacement, and this causes deterministic extinction due to minority disadvantage of reproductive interference. On the other hand, there is no deterministic extinction in the process of ecological character displacement. Furthermore, species extinction becomes less likely in the case of positive covariance between ecological and reproductive traits as divergence of the ecological trait (e.g., root depths) increases the divergence speed of the reproductive trait (e.g., flower colors) and vice versa. It will be interesting to compare intraspecific genetic (co)variance of ecological and reproductive traits in future studies for understanding how ecological and reproductive character displacement occur without extinction.     

Field and experimental evidence for competition's role in phenotypic divergence

Resource competition has long been viewed as a major cause of phenotypic divergence within and between species. Theory predicts that divergence arises because natural selection favors individuals that are phenotypically dissimilar from their competitors. Yet, there are few conclusive tests of this key prediction. Drawing on data from both natural populations and a controlled experiment, this paper presents such a test in tadpoles of two species of spadefoot toads (Spea bombifrons and S. multiplicata). These two species show exaggerated divergence in trophic morphology where they are found together (mixed-species ponds) but not where each is found alone (pure-species ponds), suggesting that they have undergone ecological character displacement. Moreover, in pure-species ponds, both species exhibit resource polymorphism. Using body size as a proxy for fitness, we found that in pure-species ponds disruptive selection favors extreme trophic phenotypes in both species, suggesting that intraspecific competition for food promotes resource polymorphism. In mixed-species ponds, by contrast, we found that trophic morphology was subject to stabilizing selection in S. multiplicata and directional selection in S. bombifrons. A controlled experiment revealed that the more similar an S. multiplicata was to its S. bombifrons tankmate in resource use, the worse was its performance. These results indicate that S. multiplicata individuals that differ from S. bombifrons would be selectively favored in competition. Our data therefore demonstrate how resource competition between phenotypically similar individuals can drive divergence between them. Moreover, our results indicate that how competition contributes to such divergence may be influenced not only by the degree to which competitors overlap in resource use, but also by the abundance and quality of resources. Finally, our finding that competitively mediated disruptive selection may promote resource polymorphism has potentially important implications for understanding how populations evolve in response to heterospecific competitors. In particular, once a population evolves resource polymorphism, it may be more prone to undergo ecological character displacement.     

Switching behavior, coexistence and diversification: comparing empirical community-wide evidence with theoretical predictions

Theory shows that the presence of behavioural switching between alternative resources can contribute to coexistence when competitors differ in trophic-related traits. In addition, switching can generate disruptive selection on such traits in a low-diversity community, increasing the number of species. Both of these processes should produce communities in which species differ in their values of the trophic trait, and display corresponding differences in the time-course of their switching from one resource to another. Here we present evidence for widespread switching behaviour for a diverse Mediterranean scrubland bird community. We show that species differ in a beak character related to their relative use of insect and fruit resource channels, and that the timing of switching is correlated with the relative use of resources. These patterns are consistent with theoretical predictions, suggesting a possible role of switching behaviour in promoting avian coexistence and diversification.     

Evaluating the targets of selection during character displacement

Ecological character displacement occurs when competition imposes divergent selection on interacting species, causing divergence in traits associated with resource use. Generally, divergence is assumed to occur when selection acts on the same, continuously varying trait in both species. However, selection might target multiple traits, and even closely related heterospecifics involved in character displacement might differ in selective targets. We investigated the targets of selection in a species of spadefoot toad, Spea multiplicata, during experimentally imposed competition with a congener, S. bombifrons. When examining traits separately, we found significant selection acting on multiple resource-acquisition traits. Yet, controlling for the independent effects of these traits in a multiple regression revealed that direct selection on a single trait might have contributed toward indirect selection on other correlated traits. Moreover, although we found evidence for plasticity in most traits, competition with S. bombifrons imposed selection on morphology and not on plasticity. Additional experiments suggest that the selective targets during character displacement might differ between the two species involved in this one instance of character displacement. Identifying the targets of competitively mediated selection is crucial, because whether and how character displacement ultimately unfolds depends on the nature of these targets and correlations among them.     

Competitive asymmetry, foraging area size and coexistence of annuals

Individuals allocate resources to the expansion of their foraging area and those resources are no longer available for the traits that determine how well those individuals are able to protect their foraging area against competitors. The resulting trade‐off between foraging area size and the traits associated with the ability to compete for the resources within the foraging area applies to ecological scenarios as different as territorial defence by individuals and colonies, and light competition in plants. Whether the trade‐off affects species performance in competition for resources at the area of overlap between foraging areas depends on the symmetry of resource division. In symmetric competition resources are divided equally between the competitors, while in asymmetric competition the individual with the smallest foraging area, and consequently the greatest competitive ability, gains all the resources. Competition may also be a combination of the symmetric and asymmetric processes. I studied the effects of competitive asymmetry on population dynamics and coexistence of two annual species with different sized foraging areas using an individual‐based spatially explicit simulation model. Symmetric competition favoured the species with the larger foraging area and did not allow coexistence. Competitive asymmetry favoured the species with smaller foraging area and allowed coexistence, which was due to the consequences of losing an asymmetric competition being more severe than losing a symmetric competition. The mechanism of coexistence is the larger foraging area's superiority in low population densities (little competition) and the smaller foraging area's ability to win a large foraging area when competition was intense. Competitive asymmetry and small size of both foraging areas led to population dynamics dominated by long‐term fluctuations of small intensity. Symmetric competition and large size of the foraging areas led to large short‐term fluctuations, which often resulted in the extinction of one or both of the species due to demographic stochasticity.     

Trait adaptation promotes species coexistence in diverse predator and prey communities

Species can adjust their traits in response to selection which may strongly influence species coexistence. Nevertheless, current theory mainly assumes distinct and time‐invariant trait values. We examined the combined effects of the range and the speed of trait adaptation on species coexistence using an innovative multispecies predator–prey model. It allows for temporal trait changes of all predator and prey species and thus simultaneous coadaptation within and among trophic levels. We show that very small or slow trait adaptation did not facilitate coexistence because the stabilizing niche differences were not sufficient to offset the fitness differences. In contrast, sufficiently large and fast trait adaptation jointly promoted stable or neutrally stable species coexistence. Continuous trait adjustments in response to selection enabled a temporally variable convergence and divergence of species traits; that is, species became temporally more similar (neutral theory) or dissimilar (niche theory) depending on the selection pressure, resulting over time in a balance between niche differences stabilizing coexistence and fitness differences promoting competitive exclusion. Furthermore, coadaptation allowed prey and predator species to cluster into different functional groups. This equalized the fitness of similar species while maintaining sufficient niche differences among functionally different species delaying or preventing competitive exclusion. In contrast to previous studies, the emergent feedback between biomass and trait dynamics enabled supersaturated coexistence for a broad range of potential trait adaptation and parameters. We conclude that accounting for trait adaptation may explain stable and supersaturated species coexistence for a broad range of environmental conditions in natural systems when the absence of such adaptive changes would preclude it. Small trait changes, coincident with those that may occur within many natural populations, greatly enlarged the number of coexisting species.     

Character displacement as the "best of a bad situation": fitness trade-offs resulting from selection to minimize resource and mate competition

Abstract Character displacement has long been considered a major cause of adaptive diversification. When species compete for resources or mates, character displacement minimizes competition by promoting divergence in phenotypes associated with resource use (ecological character displacement) or mate attraction (reproductive character displacement). In this study, we investigated whether character displacement can also have pleiotropic effects that lead to fitness trade-offs between the benefits of avoiding competition and costs accrued in other fitness components. We show that both reproductive and ecological character displacement have caused spadefoot toads to evolve smaller body size in the presence of a heterospecific competitor. Although this shift in size likely arose as a by-product of character displacement acting to promote divergence between species in mating behavior and larval development, it concomitantly reduces offspring survival, female fecundity, and sexual selection on males. Thus, character displacement may represent the "best of a bad situation" in that it lessens competition, but at a cost. Individuals in sympatry with the displaced phenotype will have higher fitness than those without the displaced trait because they experience reduced competition, but they may have reduced fitness relative to individuals in allopatry. Such a fitness trade-off can limit the conditions under which character displacement evolves and may even increase the risk of "Darwinian extinction" in sympatric populations. Consequently, character displacement may not always promote diversification in the manner that is often expected.     

Correlates of rate heterogeneity in avian ecomorphological traits

Heterogeneity in rates of trait evolution is widespread, but it remains unclear which processes drive fast and slow character divergence across global radiations. Here, we test multiple hypotheses for explaining rate variation in an ecomorphological trait (beak shape) across a globally distributed group (birds). We find low support that variation in evolutionary rates of species is correlated with life history, environmental mutagenic factors, range size, number of competitors, or living on islands. Indeed, after controlling for the negative effect of species' age, 80% of variation in species‐specific evolutionary rates remains unexplained. At the clade level, high evolutionary rates are associated with unusual phenotypes or high species richness. Taken together, these results imply that macroevolutionary rates of ecomorphological traits are governed by both ecological opportunity in distinct adaptive zones and niche differentiation among closely related species.     

Will sympatric speciation fail due to stochastic competitive exclusion?

Sympatric speciation requires coexistence of the newly formed species. If divergence proceeds by small mutational steps, the new species utilize almost the same resources initially, and full speciation may be impeded by competitive exclusion in stochastic environments. We investigate this primarily ecological problem of sympatric speciation by studying the population dynamics of a diverging asexual population in a fluctuating environment. Correlation between species responses to environmental fluctuation is assumed to decrease with distance in trait space. Rapidly declining correlation in combination with high environmental variability may delay full speciation or even render it impossible. Stochastic extinctions impeding speciation are most likely when correlation decays faster than competition, for example, when demographic stochasticity is strong or when divergence is not accompanied by niche separation, such as in speciation driven entirely by sexual selection. Our general theoretical results show an interesting connection between short-term ecological dynamics and long-term, large-scale evolution.     

Competition and evolution along environmental gradients: patterns, boundaries and sympatric divergence

The present study examined how competitive interactions and environmental conditions generate species boundaries and determine species distributions. A spatially explicit, quantitative genetic, two-species competition model was used to manipulate the strengths of competition, gene flow and local adaptation along environmental gradients. This allowed us to assess the long-term persistence of each species and whether the ranges they inhabited had boundaries in space or were unlimited. We found that a species boundary arises along less steep environmental gradients when the strength of stabilizing selection and diversifying selection are similar. We also found that a species boundary may arise along shallow environmental gradients if interspecific competition is more intense than intraspecific, which relaxes previous requirements for steep gradients for generating range limits. We determined an analytical form for the critical environmental gradient as a function of ecological and genetic parameters at which a species boundary is expected to arise by competition. Results suggest an alternative to resource competition as an explanation for phenotypic divergence between sympatric competitors. Competitors sharing a trait that is under stabilizing selection along an environmental gradient may segregate spatially and evolve in different regions, with phenotypic sympatric divergence reflecting the resulting clines. Along various types of environmental gradients, variation in stabilizing selection intensities could lead to contrasting patterns in the distribution of species. For stabilizing selection strengths in accord with field data estimates, this study predicts that the level of sympatric character divergence would be limited along environmental gradients.     

EVOLUTIONARY DIVERGENCE AND CHARACTER DISPLACEMENT IN TWO PHENOTYPICALLY-VARIABLE,COMPETING SPECIES

Theoretical studies of character displacement lead to the view that evolutionary divergence depends primarily on incomplete utilization of available resources. Those models which incorporate constraints preventing complete utilization of resources, even in the absence of competitors, all predict character displacement. Those models which allow greater flexibility of resource use within a species predict correspondingly less divergence. Indeed, Matessi and Jayakar (1980, 1981) based their conditions for occurrence of character displacement on underutilization of resources. I extend a model used by Slatkin (1980, 1983) and Taper and Case (1985) which allows each species to fully utilize its resources in the absence of competitors. I concentrate on the biologically reasonable case in which the species, though similar, differ in their ecological characteristics. As a result of this greater biological realism, I arrive at a different conclusion regarding the conditions which lead to character displacement. The presence of a variety of biological differences between species—including as a subset those which result from resource underutilization—leads to divergence with respect to a quantitatively inherited character, due to interspecific competitive interactions. The resulting displacement can be large and depends little on the parameters chosen. The only exception, involving a character with very low heritability, occurs when the non-interactive phenotypic differences are much greater than those associated with studies of character displacement in natural populations. Thus, under conditions comparable to those encountered in the field, involving similar yet not identical species, evolutionary divergence is a consequence of interspecific competition.     

ALTERNATIVE MODELS OF CHARACTER DISPLACEMENT AND NICHE SHIFT. I. ADAPTIVE SHIFTS IN RESOURCE USE WHEN THERE IS COMPETITION FOR NUTRITIONALLY NONSUBSTITUTABLE RESOURCES

This paper analyzes the influence of the nutritional status of resources on the adaptive response to interspecific competition in a consumer of those resources. The two cases compared are that in which the resources are nutritionally perfectly substitutable (in the sense of Leon and Tumpson [1975]) and that in which the resources are nonsubstitutable. Each nonsubstitutable resource must be consumed at a certain rate for population growth to occur. Evolutionarily stable strategies of resource utilization are found using models of competition for two resources. If competition occurs solely via the consumer species's effects on resource density, the adaptive response in a consumer's resource-acquisition traits is: a) divergence away from its competitor's resource-acquisition traits if resources are perfectly substitutable and b) convergence towards the competitor's resource-acquisition traits if resources are nonsubstitutable. Exceptions to both of these generalizations may occur if competitor population density affects a consumer species's per capita growth rate independently of effects on resource density. Plants and herbivores often use nonsubstitutable resources. The lack of studies of adaptive responses to competition in these organisms may be responsible for the lack of documented examples of competitive convergence.     

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.     

Experimental evolution of protozoan traits in response to interspecific competition

Decades of experiments have demonstrated the ecological effect of competition, but experimental evidence for competitive effects on trait evolution is rare. I measured the evolution of six protozoan traits in response to competitors from the inquiline community of pitcher plants. Replicate populations of Colpoda, a ciliated protozoan, were allowed to evolve in response to intra- and interspecific competition for 20 days (approximately 100 generations), before traits were measured in two common garden environments. Populations that evolved with interspecific competition had smaller cell sizes, produced fewer cysts and had higher population growth rates relative to populations grown in monoculture. The presence of interspecific competitors led to differential lineage sorting, most likely by increasing the strength of selection. These results are the first to demonstrate protozoan evolution in response to competition and may have implications for species coexistence in this system.     

Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions

Adaptive divergence of phenotypes, such as sexual dimorphism or adaptive speciation, can result from disruptive selection via competition for limited resources. Theory indicates that speciation and sexual dimorphism can result from identical ecological conditions, but co-occurrence is unlikely because whichever evolves first should dissipate the disruptive selection necessary to drive evolution of the other. Here, we consider ecological conditions in which disruptive selection can act along multiple ecological axes. Speciation in lake populations of threespine sticklebacks (Gasterosteus aculeatus) has been attributed to disruptive selection due to competition for resources. Head shape in sticklebacks is thought to reflect adaptation to different resource acquisition strategies. We measure sexual dimorphism and species variation in head shape and body size in stickleback populations in two lakes in British Columbia, Canada. We find that sexual dimorphism in head shape is greater than interspecific differences. Using a numerical simulation model that contains two axes of ecological variation, we show that speciation and sexual dimorphism can readily co-occur when the effects of loci underlying sexually dimorphic traits are orthogonal to those underlying sexually selected traits.     

Ecological release in White Sands lizards

Ecological opportunity is any change that allows populations to escape selection from competition and predation. After encountering ecological opportunity, populations may experience ecological release: enlarged population size, broadened resource use, and/or increased morphological variation. We identified ecological opportunity and tested for ecological release in three lizard colonists of White Sands, New Mexico (Sceloporus undulatus, Holbrookia maculata, and Aspidoscelis inornata). First, we provide evidence for ecological opportunity by demonstrating reduced species richness and abundance of potential competitors and predators at White Sands relative to nearby dark soils habitats. Second, we characterize ecological release at White Sands by demonstrating density compensation in the three White Sands lizard species and expanded resource use in White Sands S. undulatus. Contrary to predictions from ecological release models, we observed directional trait change but not increased trait variation in S. undulatus. Our results suggest that ecological opportunity and ecological release can be identified in natural populations, especially those that have recently colonized isolated ecosystems.     

Positive fitness consequences of interspecific interaction with a potential competitor

The coexistence of species sharing mutual resources is usually thought to be limited by negative processes such as interspecific competition. This is because an overlap in resource use leads to negative fitness consequences, and traits favouring avoidance of potential competitors, for example in habitat selection, are therefore selected for. However, species interactions are acknowledged to vary from negative (competition) to mutualism, although empirical evidence for positive interspecific interactions from natural communities of other than plants and sessile animals is scarce. Here, we experimentally examined the habitat selection and its fitness consequences of a migrant bird, the pied flycatcher (Ficedula hypoleuca), in relation to the presence of competitively superior birds, resident titmice (Parus spp.). Experiments were conducted on two spatial scales: landscape and nest-site scale. We demonstrate that pied flycatchers were attracted to and accrued fitness benefits from the presence of titmice. Flycatchers breeding in tight association with titmice initiated breeding earlier, had larger broods and heavier young than solitarily breeding flycatchers. This paradoxical result indicates that species interactions may switch from negative to positive and that the coexistence of species is not always restricted by negative costs caused by other species.     

Eco-Evolutionary dynamics enable coexistence via neighbor-dependent selection

Recent studies suggest that selection can allow coexistence in situations where ecological dynamics lead to competitive exclusion, provided that there is a trade-off between traits optimal for interacting with conspecifics and traits optimal for interacting with heterospecifics. Despite compelling empirical evidence, there is no general framework for elucidating how and when selection will allow coexistence in natural communities. Here we develop such a framework for a mechanism that we term "neighbor-dependent selection." We show that this mechanism can both augment coexistence when ecological conditions allow for niche partitioning and enable coexistence when ecological conditions lead to competitive exclusion. The novel insight is that when ecological conditions lead to exclusion, neighbor-dependent selection can allow coexistence via cycles driven by an intransitive loop; selection causes one species to be a superior interspecific competitor when it is rare and an inferior interspecific competitor when it is abundant. Our framework predicts the conditions under which selection can enable coexistence, as opposed to merely augmenting it, and elucidates the effects of heritability on the eco-evolutionary feedbacks that drive coexistence. Given increasing evidence that evolution operates on ecological timescales, our approach provides one means for evaluating the role of selection and trait evolution in species coexistence.     

Parallel evolution and ecological selection: replicated character displacement in spadefoot toads

Ecological character displacement—trait evolution stemming from selection to lessen resource competition between species—is most often inferred from a pattern in which species differ in resource-use traits in sympatry but not in allopatry, and in which sympatric populations within each species differ from conspecific allopatric populations. Yet, without information on population history, the presence of a divergent phenotype in multiple sympatric populations does not necessarily imply that there has been repeated evolution of character displacement. Instead, such a pattern may arise if there has been character displacement in a single ancestral population, followed by gene flow carrying the divergent phenotype into multiple, derived, sympatric populations. Here, we evaluate the likelihood of such historical events versus ongoing ecological selection in generating divergence in trophic morphology between multiple populations of spadefoot toad (Spea multiplicata) tadpoles that are in sympatry with a heterospecific and those that are in allopatry. We present both phylogenetic and population genetic evidence indicating that the same divergent trait, which minimizes resource competition with the heterospecific, has arisen independently in multiple sympatric populations. These data, therefore, provide strong indirect support for competition''s role in divergent trait evolution.