Character convergence under competition for nutritionally essential resources

Resource competition is thought to drive divergence in resource use traits (character displacement) by generating selection favoring individuals able to use resources unavailable to others. However, this picture assumes nutritionally substitutable resources (e.g., different prey species). When species compete for nutritionally essential resources (e.g., different nutrients), theory predicts that selection drives character convergence. We used models of two species competing for two essential resources to address several issues not considered by existing theory. The models incorporated either slow evolutionary change in resource use traits or fast physiological or behavioral change. We report four major results. First, competition always generates character convergence, but differences in resource requirements prevent competitors from evolving identical resource use traits. Second, character convergence promotes coexistence. Competing species always attain resource use traits that allow coexistence, and adaptive trait change stabilizes the ecological equilibrium. In contrast, adaptation in allopatry never preadapts species to coexist in sympatry. Third, feedbacks between ecological dynamics and trait dynamics lead to surprising dynamical trajectories such as transient divergence in resource use traits followed by subsequent convergence. Fourth, under sufficiently slow trait change, ecological dynamics often drive one of the competitors to near extinction, which would prevent realization of long-term character convergence in practice.     

Community-wide character displacement in the presence of clines: a test of Holarctic weasel guilds

1. Competition is thought to be a major influence on community assembly, ecology and evolution; presence of competitors may cause divergence in traits related to resource use (character displacement). 2. Such traits, however, often vary clinally, and this phenomenon may be independent of the presence or absence of competing species. 3. The presence of such clines can either obscure the effects of competition, or create an impression that competition is operating when, in fact, it is not. 4. We corrected for clinal variation while testing for character displacement in two well-studied weasel (Mustela) guilds, in the Nearctic and the west Palaearctic. 5. Without accounting for clines, our results agreed with previous studies suggesting character displacement in these guilds. 6. However, when we corrected for clines, predictions of competition theory were not met - and often we obtained evidence for character convergence in sympatry. 7. This may suggest that the nature of the resource base may be more important than interspecific competition in shaping morphology and size in these carnivores. 8. Our results highlight the need to account for geographic variation when studying character displacement and cast some doubt on prevailing ideas regarding the effect of competition on morphological evolution.     

What is parallelism?

Although parallel and convergent evolution are discussed extensively in technical articles and textbooks, their meaning can be overlapping, imprecise, and contradictory. The meaning of parallel evolution in much of the evolutionary literature grapples with two separate hypotheses in relation to phenotype and genotype, but often these two hypotheses have been inferred from only one hypothesis, and a number of subsidiary but problematic criteria, in relation to the phenotype. However, examples of parallel evolution of genetic traits that underpin or are at least associated with convergent phenotypes are now emerging. Four criteria for distinguishing parallelism from convergence are reviewed. All are found to be incompatible with any single proposition of homoplasy. Therefore, all homoplasy is equivalent to a broad view of convergence. Based on this concept, all phenotypic homoplasy can be described as convergence and all genotypic homoplasy as parallelism, which can be viewed as the equivalent concept of convergence for molecular data. Parallel changes of molecular traits may or may not be associated with convergent phenotypes but if so describe homoplasy at two biological levels-genotype and phenotype. Parallelism is not an alternative to convergence, but rather it entails homoplastic genetics that can be associated with and potentially explain, at the molecular level, how convergent phenotypes evolve.     

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.     

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.     

The evolution of traits affecting resource acquisition and predator vulnerability: character displacement under real and apparent competition

This article investigates some simple models of the evolutionary interaction between two prey species that share a common resource and a common predator. Each prey species is characterized by a trait that determines both the rate of resource capture and vulnerability to a predator. In a simple model of a three-species food chain, such traits usually increase in response to an imposed reduction in resource density. When the per capita growth rates of each of two prey species depend linearly on resource density, such traits will change in opposite directions when the two prey come into sympatry. In addition, the ratio of the effect of the predator on prey fitness to the effect of the resource on prey fitness will diverge from the corresponding ratio in a second prey species when those species coexist in sympatry. These simple predictions need not hold under several alternative assumptions, which may be more common in biological systems. Parallel changes in sympatry may occur if the relationship between resource consumption and prey growth is nonlinear, if the prey species have partial overlap in the set of resources used or in the set of predators that consume them, or if prey experience direct intraspecific competition. The responses to a second prey can also differ significantly from those predicted by the simplest model if separate traits affect vulnerability to predators and resource acquisition rate. It is important to determine whether examples of character displacement previously interpreted as responses to competition for resources might also reflect responses to altered predation risks in sympatry.     

Ecological and community-wide character displacement: the next generation

Ecological character displacement, mostly seen as increased differences of size in sympatry between closely‐related or similar species, is a focal hypothesis assuming that species too similar to one another could not coexist without diverging, owing to interspecific competition. Thus, ecological character displacement and community‐wide character displacement (overdispersion in size of potential competitors within ecological guilds) were at the heart of the debate regarding the role of competition in structuring ecological communities. The debate has focused on the evidence presented in earlier studies and generated a new generation of rigorous, critical studies of communities. Character displacement research in the past two decades provides sound statistical support for the hypothesis in a wide variety of taxa, albeit with a phylogenetically skewed representation. A growing number of studies are strongly based in functional morphology, and some also demonstrate actual morphologically related resource partitioning. Phylogenetic models and experimental work have added to the scope and depth of earlier research, as have theoretical studies. However, many challenging ecological and evolutionary issues, regarding both selective forces (at the inter‐ and intraspecific level) and resultant patterns, remain to be addressed. Ecological character displacement and community‐wide character displacement are here to stay as the focus of much exciting research.     

Character displacement from the receiver's perspective: species and mate recognition despite convergent signals in suboscine birds

Many social animals use long-distance signals to attract mates and defend territories. They face the twin challenges of discriminating between species to identify conspecific mates, and between individuals to recognize collaborators and competitors. It is therefore often assumed that long-distance signals are under strong selection for species-specificity and individual distinctiveness, and that this will drive character displacement when closely related species meet, particularly in noisy environments. However, the occurrence of signal stereotypy and convergence in rainforest species seems to contradict these ideas, and raises the question of whether receivers in these systems can recognize species or individuals by long-distance signals alone. Here, we test for acoustically mediated recognition in two sympatric antbird species that are known to have convergent songs. We show that male songs are stereotyped yet individually distinctive, and we use playback experiments to demonstrate that females can discriminate not only between conspecific and heterospecific males, but between mates and strangers. These findings provide clear evidence that stereotypy and convergence in male signals can be accommodated by fine tuning of perceptual abilities in female receivers, suggesting that the evolutionary forces driving divergent character displacement in animal signals are weaker than is typically assumed.     

Mixed responses to resource densities and their implications for character displacement

Summary How should a consumer of two resource types adapt to changes in their abundances? This paper shows that many different biological circumstances produce mixed responses; i.e. increasing availability of one resource increases the consumer's efforts to obtain it, while increasing availability of the other resource decreases the consumer's efforts at exploitation. This implies that competition from a second consumer species may cause convergent or divergent character displacement of the first species. The signs and magnitudes of the second derivative of the fitness function are important in determining which outcome occurs. The degree of resource limitation of the consumer species also influences the nature of adaptive shifts in resource use.     

SIGNAL DESIGN AND PERCEPTION IN HYPOCNEMIS ANTBIRDS: EVIDENCE FOR CONVERGENT EVOLUTION VIA SOCIAL SELECTION

Natural selection is known to produce convergent phenotypes through mimicry or ecological adaptation. It has also been proposed that social selection—i.e., selection exerted by social competition—may drive convergent evolution in signals mediating interspecific communication, yet this idea remains controversial. Here, we use color spectrophotometry, acoustic analyses, and playback experiments to assess the hypothesis of adaptive signal convergence in two competing nonsister taxa, Hypocnemis peruviana and H. subflava (Aves: Thamnophilidae). We show that the structure of territorial songs in males overlaps in sympatry, with some evidence of convergent character displacement. Conversely, nonterritorial vocal and visual signals in males are strikingly diagnostic, in line with 6.8% divergence in mtDNA sequences. The same pattern of variation applies to females. Finally, we show that songs in both sexes elicit strong territorial responses within and between species, whereas songs of a third, allopatric and more closely related species (H. striata) are structurally divergent and elicit weaker responses. Taken together, our results provide compelling evidence that social selection can act across species boundaries to drive convergent or parallel evolution in taxa competing for space and resources.     

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.     

Ecological character displacement caused by reproductive interference

We carried out a theoretical investigation of whether ecological character displacement can be caused by reproductive interference. Our model assumes that a quantitative character is associated with both resource use and species recognition, and that heterospecific mating incurs costs. The model shows that ecological character displacement can occur as a consequence of evolution of premating isolation; this conclusion is based on the premise that resource competition is less intense between species than within species and that the ecological character also contributes to premating isolation. When resource competition between species is intense, extinction of either species may occur by competitive exclusion before ecological character divergence. Some observational studies have shown that character displacement in body size is associated with not only resources use but also species recognition. We propose that body size displacement can occur as a consequence of evolution of premating isolation. Our results suggest that ecological character displacement results from reproductive character displacement.     

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.     

Is competition needed for ecological character displacement? Does displacement decrease competition?

Interspecific competition for resources is generally considered to be the selective force driving ecological character displacement, and displacement is assumed to reduce competition. Skeptics of the prevalence of character displacement often cite lack of evidence of competition. The present article uses a simple model to examine whether competition is needed for character displacement and whether displacement reduces competition. It treats systems with competing resources, and considers cases when only one consumer evolves. It quantifies competition using several different measures. The analysis shows that selection for divergence of consumers occurs regardless of the level of between‐resource competition or whether the indirect interaction between the consumers is competition (?,?), mutualism (+,+), or contramensalism (+,?). Also, divergent evolution always decreases the equilibrium population size of the evolving consumer. Whether divergence of one consumer reduces or increases the impact of a subsequent perturbation of the other consumer depends on the parameters and the method chosen for measuring competition. Divergence in mutualistic interactions may reduce beneficial effects of subsequent increases in the other consumer's population. The evolutionary response is driven by an increase in the relative abundance of the resource the consumer catches more rapidly. Such an increase can occur under several types of interaction.     

Positive interactions among competitors can produce species-rich communities

Although positive interactions between species are well documented, most ecological theory for investigating multispecies coexistence remains rooted in antagonistic interactions such as competition and predation. Standard resource-competition models from this theory predict that the number of coexisting species should not exceed the number of factors that limit population growth. Here I show that positive interactions among resource competitors can produce species-rich model communities supported by a single limiting resource. Simulations show that when resource competitors reduce each others' per capita mortality rate (e.g. by ameliorating an abiotic stress), stable multispecies coexistence with a single resource may be common, even while the net interspecific interaction remains negative. These results demonstrate that positive interactions may provide an important mechanism for generating species-rich communities in nature. They also show that focusing on the net interaction between species may conceal important coexistence mechanisms when species simultaneously engage in both antagonistic and positive interactions.     

Field data do not support a textbook example of convergent character displacement

Experimental evidence supporting convergent character displacement is rare; only one example exists and it is in the form of orientation and territory competition experiments performed in the laboratory. However, outcomes of laboratory experiments involving behaviour or competition can be artefacts of unnatural conditions and, therefore, the results of the previous experiments supporting convergent character displacement are equivocal. In this study, we re-examine the evolution of melanic nuptial coloration in male three-spined stickleback (Gasterosteus aculeatus) inhabiting the Chehalis River drainage in Washington State. This novel nuptial coloration has been thought to have evolved in response to competition for nesting territories with the co-distributed Olympic mudminnow (Norzumbra hubbsi), which is also melanic and breeds at the same time. I found that melanic stickleback males did not have an advantage over their red counterparts from typical populations when competing for nesting territories with Olympic mudminnows. Additionally competitive interactions between sticklebacks and mudminnows were rare in both cage experiments and naturally breeding sticklebacks. Finally, melanic coloration in the Chehalis populations did not develop until males were parental, well after the hypothesized territory establishment period. These results refute the only experimental support for convergent character displacement and emphasize the importance of conducting behavioural experiments and observations under natural conditions.     

Resource partitioning among competing species—A coevolutionary approach

A reasonably general theory for predicting the outcome of coevolution among interacting species is developed. It is applied to a model for resource partitioning among competing species.Current theory for resource partitioning is based on derivations of a “limiting similarity”—i.e., a limit to how similar competitors can be to one another consistent with coexistence. This theory presumes there is a mechanism, perhaps invasion and extinction, which causes competitors to attain the limiting similarity. The view taken in this paper is that partitioning is an evolutionary compromise between pressures for character displacement and disadvantages inherent in the shift to different resource types.A set of principles is offered for the evolution of the parameters in ecological models. (1) For single population models natural selection causes the parameters ultimately to assume those values which produce the highest equilibrium population size. (2) For models of interacting populations, but without interspecific frequency-dependence, natural selection causes the parameters to assume values which produce either the highest or lowest equilibrium population size for any species depending on the sign of the “feedback” in the community obtained by deleting that species. (3) For models of interacting populations with interspecific frequency dependence natural selection leads to parameter values which produce intermediate equilibrium population sizes. A function called the conditional equilibrium population size is introduced. Provided (a) the mean fitness is a maximum in each species at a stable coevolutionary equilibrium and (b) there is negative density-dependence in each species then natural selection causes the parameters to assume values which produce the highest conditional equilibrium population size for each species.These coevolutionary principles, applied to a model for resource partitioning, entail that the niche separation between species relative to given niche widths, increases with the variety of available resources and decreases with the number of competing populations. Also, the evolution of character displacement between two species does not proceed far enough to maximize the equilibrium population sizes of the species involved. These results imply that the relationship between the niche overlap (of nearest neighbors) and species diversity is qualitatively different depending on whether the variety of resources at any place covaries with the species diversity there. Without covariation niche overlap increases with species diversity; with covariation overlap may decrease with species diversity. This study provides the beginning of a theory for the convergent evolution of community structure.     

Competition both drives and impedes diversification in a model adaptive radiation

Competitors are known to be important in governing the outcome of evolutionary diversification during an adaptive radiation, but the precise mechanisms by which they exert their effects remain elusive. Using the model adaptive radiation of Pseudomonas fluorescens, we show experimentally that the effect of competition on diversification of a focal lineage depends on both the strength of competition and the ability of the competitors to diversify. We provide evidence that the extent of diversification in the absence of interspecific competitors depends on the strength of resource competition. We also show that the presence of competitors can actually increase diversity by increasing interspecific resource competition. Competitors that themselves are able to diversify prevent diversification of the focal lineage by removing otherwise available ecological opportunities. These results suggest that the progress of an adaptive radiation depends ultimately on the strength of resource competition, an effect that can be exaggerated or impeded by the presence of competitors.     

Adaptive responses of generalist herbivores to competition: Convergence or divergence

Summary Generalist herbivores are often faced with a choice of eating abundant, low quality foods or rare high quality foods. An adaptive forger in this situation should have mixed responses (Abrams, 1990) to the densities of the two food types. Competition from another generalist herbivore species will generally cause convergence in foraging time allocations when both species are strictly food limited. Competition will usually cause a convergent response in traits determining the relative consumption rates of the two food categories. Divergent responses are possible when consumers are not strictly food limited. Divergent responses are also expected in some other traits related to resource use, such as gut size. Evidence for the predicted responses and implications for plant-herbivore coevolution are discussed.     

Mathematical model allowing the coexistence of closely related competitors at the initial stage of evolution

The mathematical model presented here aims to elucidate the essential mechanisms of coexistence of species, especially those of closely related forms, as a result of competition in the same environment. It describes a system where the fate of the competitors or mutants is observed at the initial stage of evolution. The model encompasses both the external variables and the internal state of the competitors, which differ only in one of the metabolic rate constants. Results of simulations, even with the simplified form of the model, show that stable coexistence of closely related forms in a uniform environment is possible. In addition, the model allows the analysis of the limitations on the level of differences and similarities among the competitors for achieving a state of coexistence. The essential mechanisms for the coexistence of closely related competitors are proposed to be the involvement of the metabolic network in allowing the same growth rate of competitors which have different internal states, and the interplay between the internal states of the competitors and the external variables of their environment.