TRADE‐OFFS,SPATIAL HETEROGENEITY,AND THE MAINTENANCE OF MICROBIAL DIVERSITY

Specialization and concomitant trade‐offs are assumed to underlie the non‐neutral coexistence of lineages. Trade‐offs across heterogeneous environments can promote diversity by preventing competitive exclusion. However, the importance of trade‐offs in maintaining diversity in natural microbial assemblages is unclear, as trade‐offs are frequently not detected in artificial evolution experiments. Stressful conditions associated with patches of heavy‐metal enriched serpentine soils provide excellent opportunities for examining how heterogeneity may foster genetic diversity. Using a spatially replicated design, we demonstrate that rhizobium bacteria symbiotic with legumes inhabiting contrasting serpentine and nonserpentine soils exhibit a trade‐off between a genotype's nickel tolerance and its ability to replicate rapidly. Furthermore, we detected adaptive divergence in rhizobial assemblages across soil type heterogeneity at multiple sites, suggesting that this trade‐off may promote the coexistence of phenotypically distinct bacterial lineages. Trade‐offs and adaptive divergence may be important factors maintaining the tremendous diversity within natural assemblages of bacteria.     

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.     

Life‐history trade‐offs promote the evolution of dioecy

Most dioecious plants are perennial and subject to trade‐offs between sexual reproduction and vegetative performance. However, these broader life‐history trade‐offs have not usually been incorporated into theoretical analyses of the evolution of separate sexes. One such analysis has indicated that hermaphroditism is favoured over unisexuality when female and male sex functions involve the allocation of nonoverlapping types of resources to each sex function (e.g. allocations of carbon to female function vs. allocations of nitrogen to male function). However, some dioecious plants appear to conform to this pattern of resource allocation, with different resource types allocated to female vs. male sex functions. Using an evolutionarily stable strategy approach, we show that life‐history trade‐offs between sexual reproduction and vegetative performance enable the evolution of unisexual phenotypes even when there are no direct resource‐based trade‐offs between female and male sex functions. This result might help explain the preponderance of perennial life histories among dioecious plants and why many dioecious plants with annual life histories have indeterminate growth with ongoing trade‐offs between sexual reproduction and vegetative growth.     

Environmental context alters ecological trade‐offs controlling ant coexistence in a spatially heterogeneous region

1. Ecological trade‐offs in ant (Hymenoptera: Formicidae) assemblages and their implications for coexistence boast a rich history in entomology. Yet investigations of trade‐offs have largely been limited to homogeneous environments. We examined how environmental context modifies trade‐off expression in an ant assemblage spanning a heterogeneous region in central Florida, U.S.A. 2. We examined how trade‐off expression is altered among two contrasting habitat types: open shrub and forest. We tested for the presence of the dominance‐discovery trade‐off and two dominance‐thermal tolerance trade‐offs by estimating behavioral dominance, discovery ability, and thermal tolerance (foraging thermal limit, lethal temperature, and maximal abundance temperature) for a wide range of interacting ant species. 3. We found significantly linear dominance hierarchies in both shrub and forest habitats, showing dominant species out‐compete subordinates for food resources. In thermally stressful shrub habitats, subordinates exhibit higher thermal tolerances, take greater thermal risks, and reach maximum forager abundances at higher temperatures than do dominant species. This suggests temperature mediated trade‐offs control coexistence in shrub habitat. In thermally moderate forest habitat, we found limited evidence for trade‐offs between competitive dominance and resource discovery or between dominance and thermal traits, implying other processes control coexistence. These results demonstrate that trade‐offs controlling ant coexistence may be contingent on environmental context.     

Resource competition and adaptive radiation in a microbial microcosm

Theory predicts that competition for shared resources in a monomorphic population generates divergent selection for adaptation to alternative resources. Experimental tests of this hypothesis are scarce. We selected populations of the bacterium Pseudomonas fluorescens in spatially homogeneous microcosms containing a complex mixture of resources. Initially, all populations consisted of two isogenic clones. The outcome of selection was the evolution of a diverse community of genotypes within each population. Sympatric genotypes exhibited differentiation in metabolic traits related to resource acquisition and frequency‐dependent trade‐offs in competitive ability, as we would expect if different genotypes consumed different resources. These results are consistent with the hypothesis of adaptive radiation driven by resource competition. Reconciling the results of this study with those of earlier experiments provides a new interpretation of the ecological causes of adaptive radiation in microbial microcosms.     

EVOLUTION OF THE STORAGE EFFECT

The storage effect, a mechanism that promotes species coexistence in temporally variable environments, poses a dilemma to evolutionary ecologists. Ecological studies have demonstrated its importance in natural communities, but evolutionary models have predicted that selection either impedes coexistence or diminishes the storage effect if there is coexistence. Here, we develop a lottery model of competition in which two species experience a trade‐off in competitive ability between two types of years. We use an adaptive evolution framework to determine conditions favoring the evolution of the storage effect. Storage evolves via divergence of relative performance in the two environments under a wide range of biologically realistic conditions. It evolves between two initially identical species (or lineages) when the trade‐off in performance is strong enough. It evolves for species having different initial trade‐offs for both weak and strong trade‐offs. Our simple 2‐species‐2‐environment scenario can be extended to multiple species and environmental conditions. Results indicate that the storage effect should evolve in a broad range of situations that involve a trade‐off in competitive ability among years, and are consistent with empirical observations. The findings show that storage can evolve in a manner and under conditions similar to other types of resource partitioning.     

Coexistence and displacement in consumer-resource systems with local and shared resources

Competition for local and shared resources is widespread. For example, colonial waterbirds consume local prey in the immediate vicinity of their colony, as well as shared prey across multiple colonies. However, there is little understanding of conditions facilitating coexistence vs. displacement in such systems. Extending traditional models based on type I and type II functional responses, we simulate consumer-resource systems in which resources are “substitutable,” “essential,” or “complementary.” It is shown that when resources are complementary or essential, a small increase in carrying capacity or decrease in handling time of a local resource may displace a spatially separate consumer species, even when the effect on shared resources is small. This work underscores the importance of determining both the nature of resource competition (substitutable, essential, or complementary) and appropriate scale-dependencies when studying metacommunities. We discuss model applicability to complex systems, e.g., urban wildlife that consume natural and anthropogenic resources which may displace rural competitors by depleting shared prey.     

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, ??, ??–??.     

A negative heterogeneity–diversity relationship found in experimental grassland communities

Recent meta-analyses and simulation studies have suggested that the relationship between soil resource heterogeneity and plant diversity (heterogeneity–diversity relationship; HDR) may be negative when heterogeneity occurs at small spatial scales. To explore different mechanisms that can explain a negative HDR, we conducted a mesocosm experiment combining a gradient of soil nutrient availability (low, medium, high) and scale of heterogeneity (homogeneous, large-scale heterogeneous, small-scale heterogeneous). The two heterogeneous treatments were created using chessboard combinations of low and high fertility patches, and had the same overall fertility as the homogeneous medium treatment. Soil patches were designed to be relatively larger (156 cm²) and smaller (39 cm²) than plant root extent. We found plant diversity was significantly lower in the small-scale heterogeneous treatment compared to the homogeneous treatment of the same fertility. Additionally, low fertility patches in the small-scale heterogeneous treatment had lower diversity than patches of the same size in the low fertility treatment. Shoot and root biomass were larger in the small-scale heterogeneous treatment than in the homogeneous treatment of the same fertility. Further, we found that soil resource heterogeneity may reduce diversity indirectly by increasing shoot biomass, thereby enhancing asymmetric competition for light resources. When soil resource heterogeneity occurs at small spatial scales it can lower plant diversity by increasing asymmetric competition belowground, since plants with large root systems can forage among patches and exploit soil resources. Additionally, small-scale soil heterogeneity may lower diversity indirectly, through increasing light competition, when nutrient uptake by competitive species increases shoot biomass production.     

Experimental evolution for generalists and specialists reveals multivariate genetic constraints on thermal reaction norms

Theory predicts the emergence of generalists in variable environments and antagonistic pleiotropy to favour specialists in constant environments, but empirical data seldom support such generalist–specialist trade‐offs. We selected for generalists and specialists in the dung fly Sepsis punctum (Diptera: Sepsidae) under conditions that we predicted would reveal antagonistic pleiotropy and multivariate trade‐offs underlying thermal reaction norms for juvenile development. We performed replicated laboratory evolution using four treatments: adaptation at a hot (31 °C) or a cold (15 °C) temperature, or under regimes fluctuating between these temperatures, either within or between generations. After 20 generations, we assessed parental effects and genetic responses of thermal reaction norms for three correlated life‐history traits: size at maturity, juvenile growth rate and juvenile survival. We find evidence for antagonistic pleiotropy for performance at hot and cold temperatures, and a temperature‐mediated trade‐off between juvenile survival and size at maturity, suggesting that trade‐offs associated with environmental tolerance can arise via intensified evolutionary compromises between genetically correlated traits. However, despite this antagonistic pleiotropy, we found no support for the evolution of increased thermal tolerance breadth at the expense of reduced maximal performance, suggesting low genetic variance in the generalist–specialist dimension.     

Multi‐scale responses to warming in an experimental insect metacommunity

In metacommunities, diversity is the product of species interactions at the local scale and dispersal between habitat patches at the regional scale. Although warming can alter both species interactions and dispersal, the combined effects of warming on these two processes remains uncertain. To determine the independent and interactive effects of warming‐induced changes to local species interactions and dispersal, we constructed experimental metacommunities consisting of enclosed milkweed patches seeded with five herbivorous milkweed specialist insect species. We treated metacommunities with two levels of warming (unwarmed and warmed) and three levels of connectivity (isolated, low connectivity, high connectivity). Based on metabolic theory, we predicted that if plant resources were limited, warming would accelerate resource drawdown, causing local insect declines and increasing both insect dispersal and the importance of connectivity to neighboring patches for insect persistence. Conversely, given abundant resources, warming could have positive local effects on insects, and the risk of traversing a corridor to reach a neighboring patch could outweigh the benefits of additional resources. We found support for the latter scenario. Neither resource drawdown nor the weak insect‐insect associations in our system were affected by warming, and most insect species did better locally in warmed conditions and had dispersal responses that were unchanged or indirectly affected by warming. Dispersal across the matrix posed a species‐specific risk that led to declines in two species in connected metacommunities. Combined, this scaled up to cause an interactive effect of warming and connectivity on diversity, with unwarmed metacommunities with low connectivity incurring the most rapid declines in diversity. Overall, this study demonstrates the importance of integrating the complex outcomes of species interactions and spatial structure in understanding community response to climate change.     

Parallelism in adaptive radiations of experimental Escherichia coli populations

Adaptive radiations are major contributors to species diversity. Although the underlying mechanisms of adaptive radiations, specialization and trade‐offs, are relatively well understood, the tempo and repeatability of adaptive radiations remain elusive. Ecological specialization can occur through the expansion into novel niches or through partitioning of an existing niche. To test how the mode of resource specialization affects the tempo and repeatability of adaptive radiations, we selected replicate bacterial populations in environments that promoted the evolution of diversity either through niche expansion or through niche partitioning, and in a third low‐quality single‐resource environment, in which diversity was not expected to evolve. Colony size diversity evolved equally fast in environments that provided ecological opportunities regardless of the mode of resource specialization. In the low‐quality environments, diversity did not consistently evolve. We observed the largest fitness improvement in the low‐quality environment and the smallest the glucose‐limited environment. We did not observe a change in the rate of evolutionary change in either trait or environment, suggesting that the pool of beneficial mutations was not exhausted. Overall, the mode of resource specialization did not affect the tempo or repeatability of adaptive radiations. These results demonstrate the limitations of eco‐evolutionary feedbacks to affect evolutionary outcomes.     

The effect of spatial heterogeneity and parasites on the evolution of host diversity

Both spatial heterogeneity and exploiters (parasites and predators) have been implicated as key ecological factors driving population diversification. However, it is unclear how these factors interact. We addressed this question using the common plant-colonizing bacterium Pseudomonas fluorescens, which has been shown to diversify rapidly into spatial niche-specialist genotypes when propagated in laboratory microcosms. Replicate populations were evolved in spatially homogeneous and heterogeneous environments (shaken and static microcosms, respectively) with and without viral parasites (bacteriophage) for approximately 60 bacterial generations. Consistent with previous findings, exploiters reduced diversity in heterogeneous environments by relaxing the intensity of resource competition. By contrast, exploiters increased diversity in homogeneous environments where there was little diversification through resource competition. Competition experiments revealed this increase in diversity to be the result of fitness trade-offs between exploiter resistance and competitive ability. In both environments, exploiters increased allopatric diversity, presumably as a result of divergent selection for resistance between populations. Phage increased total diversity in homogeneous environments, but had no net effect in heterogeneous environments. Such interactions between key ecological variables need to be considered when addressing diversification and coexistence in future studies.     

Evolution of the leaf economics spectrum in herbs: Evidence from environmental divergences in leaf physiology across Helianthus (Asteraceae)

The leaf economics spectrum (LES) describes a major axis of plant functional trait variation worldwide, defining suites of leaf traits aligned with resource‐acquisitive to resource‐conservative ecological strategies. The LES has been interpreted to arise from leaf‐level trade‐offs among ecophysiological traits common to all plants. However, it has been suggested that the defining leaf‐level trade‐offs of the LES may not hold within specific functional groups (e.g., herbs) nor within many groups of closely related species, which challenges the usefulness of the LES paradigm across evolutionary scales. Here, we examine the evolution of the LES across 28 species of the diverse herbaceous genus Helianthus (the sunflowers), which occupies a wide range of habitats and climate variation across North America. Using a phylogenetic comparative approach, we find repeated evolution of more resource‐acquisitive LES strategies in cooler, drier, and more fertile environments. We also find macroevolutionary correlations among LES traits that recapitulate aspects of the global LES, but with one major difference: leaf mass per area is uncorrelated with leaf lifespan. This indicates that whole‐plant processes likely drive variation in leaf lifespan across Helianthus, rather than leaf‐level trade‐offs. These results suggest that LES patterns do not reflect universal physiological trade‐offs at small evolutionary scales.     

Optimal cell size for resource uptake in fluids: a new facet of resource competition

Planktonic microorganisms are affected by various size-dependent processes both from the bottom up and from the top down. We developed a simple resource-consumer model to explore how size-dependent resource uptake and resource loss influence the growth of, and competition between, planktonic microorganisms. We considered three steps of resource uptake: diffusive transport of resource molecules, uptake by membrane transporters, and cellular enzymatic catalysis, and we investigated optimal cell size when one, two, or three of those steps limit resource uptake. Optimal cell size depends negatively on the size of resource molecules when resource uptake is limited by diffusive transport and membrane uptake. When competing for two resources of different molecular sizes, two different-sized consumers can coexist if the inputs of resources and sizes of consumers are correctly chosen. The model suggests that mixtures of various-sized resources can promote coexistence and size diversity of microorganisms even if the availability of one element, such as carbon, nitrogen, or phosphorus, limits the whole community. Model predictions include that bacteria grown on maltose or polysaccharides should be smaller compared with those grown on glucose under carbon limitation. Our results suggest that size of resource molecules can be an important factor in microbial resource competition in aquatic environments.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

Effects of variation in resource acquisition during different stages of the life cycle on life‐history traits and trade‐offs in a burying beetle

Individual variation in resource acquisition should have consequences for life‐history traits and trade‐offs between them because such variation determines how many resources can be allocated to different life‐history functions, such as growth, survival and reproduction. Since resource acquisition can vary across an individual's life cycle, the consequences for life‐history traits and trade‐offs may depend on when during the life cycle resources are limited. We tested for differential and/or interactive effects of variation in resource acquisition in the burying beetle Nicrophorus vespilloides. We designed an experiment in which individuals acquired high or low amounts of resources across three stages of the life cycle: larval development, prior to breeding and the onset of breeding in a fully crossed design. Resource acquisition during larval development and prior to breeding affected egg size and offspring survival, respectively. Meanwhile, resource acquisition at the onset of breeding affected size and number of both eggs and offspring. In addition, there were interactive effects between resource acquisition at different stages on egg size and offspring survival. However, only when females acquired few resources at the onset of breeding was there evidence for a trade‐off between offspring size and number. Our results demonstrate that individual variation in resource acquisition during different stages of the life cycle has important consequences for life‐history traits but limited effects on trade‐offs. This suggests that in species that acquire a fixed‐sized resource at the onset of breeding, the size of this resource has larger effects on life‐history trade‐offs than resources acquired at earlier stages.     

The influence of multiple functional demands on morphological diversification: A test on turtle shells

Organismal parts are often involved in the performance of more than one function. The role of trade‐offs in influencing phenotypic evolution of such parts is well‐studied; less well‐understood is their role in influencing phenotypic diversity. Increases in the number of functions a part is involved in may inhibit subsequent diversification, as the number of trade‐offs increases. Alternately, such an increase might promote phenotypic diversification, by increasing adaptive landscape complexity and promoting specialization for different roles. We compare these predictions by testing whether aquatic turtle shells, which resist loads, act as hydrodynamic elements, facilitate self‐righting, and exchange heat with the environment, differ in phenotypic diversity from those of terrestrial species, which perform all the same functions except for hydrodynamics. We used 53 3D landmarks digitized on 2722 specimens of 274 hard‐shelled turtle species to quantify shell shape variation, and a set of phylogenetic hypotheses to examine evolutionary patterns. Terrestrial turtles consistently had higher phenotypic diversity than aquatic species. Differences are not due to differences in the rates of evolution between the two groups, but rather differences in evolutionary mode. Thus this study supports the traditional view of the role of multiple functions in determining phenotypic diversity.     

SIGN EPISTASIS LIMITS EVOLUTIONARY TRADE‐OFFS AT THE CONFLUENCE OF SINGLE‐ AND MULTI‐CARBON METABOLISM IN METHYLOBACTERIUM EXTORQUENS AM1

Adaptation of one set of traits is often accompanied by attenuation of traits important in other selective environments, leading to fitness trade‐offs. The mechanisms that either promote or prevent the emergence of trade‐offs remain largely unknown, and are difficult to discern in most systems. Here, we investigate the basis of trade‐offs that emerged during experimental evolution of Methylobacterium extorquens AM1 to distinct growth substrates. After 1500 generations of adaptation to a multi‐carbon substrate, succinate (S), many lineages had lost the ability to use one‐carbon compounds such as methanol (M), generating a mixture of M⁺ and M^? evolved phenotypes. We show that trade‐offs in M^? strains consistently arise via antagonistic pleiotropy through recurrent selection for loss‐of‐function mutations to ftfL (formate‐tetrahydrofolate ligase), which improved growth on S while simultaneously eliminating growth on M. But if loss of FtfL was beneficial, why were M trade‐offs not found in all populations? We discovered that eliminating FtfL was not universally beneficial on S, as it was neutral or even deleterious in certain evolved lineages that remained M⁺. This suggests that sign epistasis with earlier arising mutations prevented the emergence of mutations that drove trade‐offs through antagonistic pleiotropy, limiting the evolution of metabolic specialists in some populations.     

Trade-offs in community ecology: linking spatial scales and species coexistence

Trade‐offs in species performances of different ecological functions is one of the most common explanations for coexistence in communities. Despite the potential for species coexistence occurring at local or regional spatial scales, trade‐offs are typically approached at a single scale. In recent years, ecologists have increasingly provided evidence for the importance of community processes at both local and regional spatial scales. This review summarizes the theoretical predictions for the traits associated with trade‐offs under different conditions and at different spatial scales. We provide a spatial framework for understanding trade‐offs, coexistence and the supportive empirical evidence. Predictions are presented that link the patterns of diversity observed to the patterns of trade‐offs that lead to coexistence at different spatial scales. Recent evidence for the evolution of trade‐offs under different conditions is provided which explores both laboratory microcosm studies and phylogenetic tests. Examining trade‐offs within a spatial framework can provide a strong approach to understanding community structure and dynamics, while explaining patterns of species diversity.