Advantage of storage in a fluctuating environment

We will elaborate the evolutionary course of an ecosystem consisting of a population in a chemostat environment with periodically fluctuating nutrient supply. The organisms that make up the population consist of structural biomass and energy storage compartments. In a constant chemostat environment a species without energy storage always out-competes a species with energy reserves. This hinders evolution of species with storage from those without storage. Using the adaptive dynamics approach for non-equilibrium ecological systems we will show that in a fluctuating environment there are multiple stable evolutionary singular strategies (ss's): one for a species without, and one for a species with energy storage. The evolutionary end-point depends on the initial evolutionary state. We will formulate the invasion fitness in terms of Floquet multipliers for the oscillating non-autonomous system. Bifurcation theory is used to study points where due to evolutionary development by mutational steps, the long-term dynamics of the ecological system changes qualitatively. To that end, at the ecological time scale, the trait value at which invasion of a mutant into a resident population becomes possible can be calculated using numerical bifurcation analysis where the trait is used as the free parameter, because it is just a bifurcation point. In a constant environment there is a unique stable equilibrium for one species following the "competitive exclusion" principle. In contrast, due to the oscillatory dynamics on the ecological time scale two species may coexist. That is, non-equilibrium dynamics enhances biodiversity. However, we will show that this coexistence is not stable on the evolutionary time scale and always one single species survives.     

Death and cannibalism in a seasonal environment facilitate bacterial coexistence

Bacterial populations can evolve and adapt to become diverse niche specialists, even in seemingly homogeneous environments. One source of this diversity arises from newly 'constructed' niches that result from the activities of the bacteria themselves. Ecotypes specialized to exploit these distinct niches can subsequently coexist via frequency-dependent interactions. Here, we describe a novel form of niche construction that is based upon differential death and cannibalism, and which evolved during 20 000 generations of experimental evolution in Escherichia coli in a seasonal environment with alternating growth and starvation. In one of 12 populations, two monophyletic ecotypes, S and L, evolved that stably coexist with one another. When grown and then starved in monoculture, the death rate of S exceeds that of L, whereas the reverse is observed in mixed cultures. As shown by experiments and numerical simulations, the competitive advantage of S cells is increased by extending the period of starvation, and this advantage results from their cannibalization of the debris of lysed L cells, which allows the S cells to increase both their growth rate and total cell density. At the molecular level, the polymorphism is associated with divergence in the activity of the alternative sigma factor RpoS, with S cells displaying no detectable activity, while L cells show increased activity relative to the ancestral genotype. Our results extend the repertoire of known cross-feeding mechanisms in microbes to include cannibalism during starvation, and confirm the central roles for niche construction and seasonality in the maintenance of microbial polymorphisms.     

Evolution of specialization in resource utilization in structured metapopulations

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

Competitive coexistence in spatially structured environments: a synthesis

Theoretical developments in spatial competitive coexistence are far in advance of empirical investigations. A framework that makes comparative predictions for alternative hypotheses is a crucial element in narrowing this gap. This review attempts to synthesize spatial competition theory into such a framework, with the goal of motivating empirical investigations that adopt the comparative approach. The synthesis presented is based on a major axis, coexistence in spatially homogeneous vs. heterogeneous competitive environments, along which the theory can be organized. The resulting framework integrates such key concepts as niche theory, spatial heterogeneity and spatial scale(s) of coexistence. It yields comparative predictions that can guide empirical investigations.     

生态群落物种共存的进化机制

本文概述了目前对生态群落的物种共存研究中存在的若干问题及动、植物群落物种共存机制的研究进展。植物群落的物种共存主要介绍与环境、种子再迁移、生态位分化、竞争平衡理论、种库假设、再生生态位等有关的几种假设、生态学上相似种的共存及“原”群落概念等。动物群落的物种共存机制主要从以下几方面叙述：（1）异质环境中的资源分割,主要指动物斑状滋养的不同利用;（2）避免竞争排斥的行为机制,如边缘效应、聚群效应、扩散行为、相互作用和干扰;（3）特化者和泛化者的共存,包括：竞争是物种向多功能进化的作用力、最佳觅食理论与生态学特化及特化概念的发展。最后指出进一步研究的方向。     

Evolution of a plastic quantitative trait in an age-structured population in a fluctuating environment

We analyze weak fluctuating selection on a quantitative character in an age-structured population not subject to density regulation. We assume that early in the first year of life before selection, during a critical state of development, environments exert a plastic effect on the phenotype, which remains constant throughout the life of an individual. Age-specific selection on the character affects survival and fecundity, which have intermediate optima subject to temporal environmental fluctuations with directional selection in some age classes as special cases. Weighting individuals by their reproductive value, as suggested by Fisher, we show that the expected response per year in the weighted mean character has the same form as for models with no age structure. Environmental stochasticity generates stochastic fluctuations in the weighted mean character following a first-order autoregressive model with a temporally autocorrelated noise term and stationary variance depending on the amount of phenotypic plasticity. The parameters of the process are simple weighted averages of parameters used to describe age-specific survival and fecundity. The "age-specific selective weights" are related to the stable distribution of reproductive values among age classes. This allows partitioning of the change in the weighted mean character into age-specific components.     

Evolution of handling time can destroy the coexistence of cycling predators

Several consumers (predators) with Holling type II functional response may robustly coexist even if they utilize the same resource (prey), provided that the population exhibits nonequilibrium dynamics and the handling time of predators is sufficiently different. We investigate the evolution of handling time and, in particular, its effect on coexistence. Longer handling time is costly in terms of lost foraging time, but allows more nutrients to be extracted from a captured prey individual. Assuming a hyperbolically saturating relationship between handling time and the number of new predators produced per prey consumed, we obtain three results: (i) There is a globally evolutionarily stable handling time; (ii) At most two predator strategies can coexist in this model; (iii) When two predators coexist, a mutant with intermediate handling time can always invade. This implies that there is no evolutionarily stable coexistence, and the evolution of handling time eventually leads to a single evolutionarily stable predator. These results are proven analytically and are valid for arbitrary (not only small) mutations; they however depend on the relationship between handling time and offspring production and on the assumption that predators differ only in their prey handling strategy.     

Mechanisms of coexistence of a bacteria and a bacteriophage in a spatially homogeneous environment

When bacteriophage are added to laboratory bacteria populations, bacteria mutants that are resistant to the phage quickly dominate the population. The phage will only persist in the long‐term if there are sufficient bacteria in the population that show susceptibility to the phage. We investigated the mechanisms allowing for coexistence by adding the virulent bacteriophage φ6 to cultures of the bacterium Pseudomonas syringae pv. phaseolicola in a spatially homogeneous environment. We saw large differences between replicate cultures, in particular when one or both of the species persisted. These differences can be explained by variation in the timing of the appearance of various resistant phenotypes in the bacteria populations before the phage were added, which determines their relative frequencies within the populations. Although these resistant phenotypes have similar fitnesses in the presence and in the absence of the phage, they have a profound effect on the persistence of the phage. Our results give a clearer understanding of the ecological mechanisms that lead to the coexistence of bacteria and virulent phage in environments where there are no spatial refuges available to the bacteria population.     

Population models in a periodically fluctuating environment

Summary We investigate the behavior of population models in the presence of a periodically fluctuating environment. We consider in particular single-species models and models of interspecific competition. It is shown that the fluctuations cause constant equilibrium states to be replaced by periodic equilibrium states, with a shift in the mean value relative to the constant-environment state. It is shown also that the locations of points of exchange of stability may be changed as a result of the fluctuations.     

Selection in a fluctuating environment leads to decreased genetic variation and facilitates the evolution of phenotypic plasticity

Changes in the environment are expected to induce changes in the quantitative genetic variation, which influences the ability of a population to adapt to environmental change. Furthermore, environmental changes are not constant in time, but fluctuate. Here, we investigate the effect of rapid, continuous and/or fluctuating temperature changes in the seed beetle Callosobruchus maculatus, using an evolution experiment followed by a split-brood experiment. In line with expectations, individuals responded in a plastic way and had an overall higher potential to respond to selection after a rapid change in the environment. After selection in an environment with increasing temperature, plasticity remained unchanged (or decreased) and environmental variation decreased, especially when fluctuations were added; these results were unexpected. As expected, the genetic variation decreased after fluctuating selection. Our results suggest that fluctuations in the environment have major impact on the response of a population to environmental change; in a highly variable environment with low predictability, a plastic response might not be beneficial and the response is genetically and environmentally canalized resulting in a low potential to respond to selection and low environmental sensitivity. Interestingly, we found greater variation for phenotypic plasticity after selection, suggesting that the potential for plasticity to evolve is facilitated after exposure to environmental fluctuations. Our study highlights that environmental fluctuations should be considered when investigating the response of a population to environmental change.     

Eco-evolutionary maintenance of diversity in fluctuating environments

Growing evidence suggests that temporally fluctuating environments are important in maintaining variation both within and between species. To date, however, studies of genetic variation within a population have been largely conducted by evolutionary biologists (particularly population geneticists), while population and community ecologists have concentrated more on diversity at the species level. Despite considerable conceptual overlap, the commonalities and differences of these two alternative paradigms have yet to come under close scrutiny. Here, we review theoretical and empirical studies in population genetics and community ecology focusing on the ‘temporal storage effect’ and synthesise theories of diversity maintenance across different levels of biological organisation. Drawing on Chesson's coexistence theory, we explain how temporally fluctuating environments promote the maintenance of genetic variation and species diversity. We propose a further synthesis of the two disciplines by comparing models employing traditional frequency-dependent dynamics and those adopting density-dependent dynamics. We then address how temporal fluctuations promote genetic and species diversity simultaneously via rapid evolution and eco-evolutionary dynamics. Comparing and synthesising ecological and evolutionary approaches will accelerate our understanding of diversity maintenance in nature.     

On the emergence of primitive cooperation in an environment of fluctuating resource supply

A necessary property of cooperative behaviour in the animal kingdom is the reciprocal (or multilateral) dependence of the animals on one another for the purpose of (joint) competition for limited resources. The emergence of such patterns of dependent behaviour, whether cooperative or not, is often concurrent with the emergence of communication structures between the animals. Animal communication is always local, thus introducing an aspect of spatial localization into an otherwise homogenous population (deme structure, Wright 1945). In order to investigate the relation between emergent cooperation and communication, we introduce a model of primitive organisms living and reproducing in colonies (demes) connected by migration. Different migration structures are considered. Exposed to an environment in which the food resource supply is not deterministically fixed but stochastic, we first investigate whether the resulting supply uncertainty adversely affects the total carrying capacity of the colonies. We show that this is not always the case and provide a necessary and sufficient criterion. Modelling the supply uncertainty by a simple Markov process, we next explore whether a certain type of emergent communication (e.g. communication by means of waste metabolites) helps reverse the potentially adverse effect of food supply uncertainty. We distinguish between excitatory and inhibitory signalling and show that in the context of our model it is the inhibitory interpretation which provides the selective advantage. It will be shown that the higher the fidelity of the transmitted information, the larger the fitness differential derived. The paper develops a useful combination of (elementary) perturbation and stochastic averaging techniques (the first order dynamics is used to average second order terms) which may be of interest outside the application reported here.     

Transients and tradeoffs of phenotypic switching in a fluctuating limited environment

Phenotypic variability in a microorganism population is thought to be advantageous in fluctuating environments, however much remains unknown about the precise conditions for this advantage to hold. In particular competition for a growth-limiting resource and the dynamics of that resource in the environment modify the tradeoff between different effects of variability. Here we investigate theoretically a model system for variable populations under competition for a flowing resource that governs growth (chemostat model) and changes with time. This environment generally induces density-dependent selection among competing sub-populations. We characterize quantitatively the transient dynamics in this system, and find that equilibration between total population density and environment can occur separately and with a distinct timescale from equilibration between competing sub-populations. We analyze quantitatively the two opposing effects of heterogeneity-transient response to change, and fitness at equilibrium-and find the optimal strategy in a fluctuating environment. We characterize the phase diagram of the system in term of its optimal strategy and find it to be strongly dependent on the typical timescale of the environment and weakly dependent on the internal parameters of the population.     

Trade-Offs Predicted by Metabolic Network Structure Give Rise to Evolutionary Specialization and Phenotypic Diversification

Mitigating trade-offs between different resource-utilization functions is key to an organism’s ecological and evolutionary success. These trade-offs often reflect metabolic constraints with a complex molecular underpinning; therefore, their consequences for evolutionary processes have remained elusive. Here, we investigate how metabolic architecture induces resource-utilization constraints and how these constraints, in turn, elicit evolutionary specialization and diversification. Guided by the metabolic network structure of the bacterium Lactococcus cremoris, we selected two carbon sources (fructose and galactose) with predicted coutilization constraints. By evolving L. cremoris on either fructose, galactose, or a mix of both sugars, we imposed selection favoring divergent metabolic specializations or coutilization of both resources, respectively. Phenotypic characterization revealed the evolution of either fructose or galactose specialists in the single-sugar treatments. In the mixed-sugar regime, we observed adaptive diversification: both specialists coexisted, and no generalist evolved. Divergence from the ancestral phenotype occurred at key pathway junctions in the central carbon metabolism. Fructose specialists evolved mutations in the fbp and pfk genes that appear to balance anabolic and catabolic carbon fluxes. Galactose specialists evolved increased expression of pgmA (the primary metabolic bottleneck of galactose metabolism) and silencing of ptnABCD (the main glucose transporter) and ldh (regulator/enzyme of downstream carbon metabolism). Overall, our study shows how metabolic network architecture and historical contingency serve to predict targets of selection and inform the functional interpretation of evolved mutations. The elucidation of the relationship between molecular constraints and phenotypic trade-offs contributes to an integrative understanding of evolutionary specialization and diversification.     

Integrating nested spatial scales: implications for the coexistence of competitors on a patchy resource

1. Intraspecific aggregation at a single spatial scale can promote the coexistence of competitors. This paper demonstrates how this same mechanism can be applied to the many systems that are patchy at two scales, with patches nested within 'superpatches'.
2. Data are presented from a field study showing that insects living in rotting fruits have aggregated distributions in the fruits under a single tree, and that the mean density and degree of aggregation varies significantly among trees. Observations in this system motivate the following models.
3. A model of competition has been developed between two species which explicitly represents spatial variation at two scales. By integrating the probability distributions for each scale, the marginal distributions of competitors over all patches can be found and used to calculate coexistence criteria. This model assumes global movement of the competitors.
4. Although spatial variation at a single scale may not be sufficient for coexistence, the total variation over all patches can allow coexistence. Variation in mean densities among superpatches and variation in the degree of aggregation among superpatches both promote coexistence, but act in different ways.
5. A second model of competition between two species is described which incorporates the effects of limited movement among superpatches. Limited movement among superpatches generally promotes coexistence, and also leads to correlations among aggregation and the mean densities of competitors.     

Evolution of specialization in a spatially continuous environment

We study the evolution of specialization in a spatially continuous (one‐dimensional) environment divided into two habitats; we use a general trade‐off function relating fitnesses in the two habitats and illustrate our results with two classical trade‐off functions. We show that the population can either reach an intermediate value of the trait and be moderately adapted to both habitats (1 generalist), or split into two locally adapted subpopulations (2 specialists). We recover the qualitative results obtained with simpler metapopulation models with island migration: the evolutionary outcome depends on the concavity of the trade‐off, on the proportion of each habitat and on migration. Our quantitative prediction on migration, however, depends on isolation by distance. Our spatially explicit model may thus be particularly useful to describe the evolutionary dynamics of specialization in, perhaps, more realistic ecological scenarios.     

Impacts of dispersal on rapid adaptation and dynamic stability of Daphnia in fluctuating environments

Prior ecological research has shown that spatial processes can enhance the temporal stability of populations in fluctuating environments. Less explored is the effect of dispersal on rapid adaptation and its concomitant impact on population dynamics. For asexually reproducing populations, theory predicts that dispersal in fluctuating environments can facilitate asynchrony among clones and enhance stability by reducing temporal variability of total population abundance. This effect is predicted when clones exhibit heritable variation in environmental optima and when fluctuations occur asynchronously among patches. We tested this in the field using artificial ponds and metapopulations composed of a diverse assemblage of Daphnia pulex clones. We directly manipulated dispersal presence/absence and environmental fluctuations in the form of nutrient pulses. Consistent with predictions, dispersal enhanced temporal asynchrony among clones in the presence of nutrient pulses; this in turn stabilized population dynamics. This effect only emerged when patches experienced spatially asynchronous nutrient pulses (dispersal had no effect when patches were synchronously pulsed). Clonal asynchrony was driven by strong positive selection for a single clone that exhibited a performance advantage under conditions of low resource availability. Our work highlights the importance of dispersal as a driver of eco-evolutionary dynamics and population stability in variable environments.     

Demographic mechanisms in the coexistence of two closely related perennials in a fluctuating environment

The demographic variability and life history differentiation of two closely related shrubs (Atriplex canescens and A. acanthocarpa) were investigated in the Chihuahuan Desert, and the results were interpreted in the context of theories of coexistence in fluctuating environments. Demographic information was recorded during three annual intervals and analyzed employing matrix projection models. A. canescens had lower λ (finite rate of population increase), higher longevity and generation time and slower convergence to a stable population structure than A. acanthocarpa. In favorable years for recruitment (those when, for both species, λ > 1), the λ of A. acanthocarpa was higher than that of A. canescens; in unfavorable years (when λ < 1), the reverse was true. Regardless of conditions (year), A. acanthocarpa had a type 2 survivorship curve (constant rate of mortality with age), while A. canescens had a type 3 survivorship curve (declining mortality with age). Elasticity analyses highlighted the larger influence that fecundity and growth would have in modifying the λ of A. acanthocarpa in comparison to that of A. canescens. In contrast, survival would have a larger influence on the λ of A. canescens. Atriplex acanthocarpa behaved as an opportunistic species that benefitted from sporadic favorable conditions and declined rapidly when conditions deteriorated. In contrast, A. canescens behaved as a tolerant species able to withstand years when conditions were poor, but which could not gain any advantage over A. acanthocarpa when conditions improved. By each having a relative advantage over the other on opposite ends of the contrasting climatic conditions experienced in the Chihuahuan Desert, they are able to coexist. Their contrasting life histories agreed with the theoretical predictions for the operation of the two mechanisms of species coexistence in fluctuating environments: the storage effect and the relative non-linearity of competition. Based on these results, we conclude by speculating on the nature of succession in arid communities.     

Trade-off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions

Explanations of floral adaptation to diverse pollinator faunas have often invoked visitor-mediated trade-offs in which no intermediate, generalized floral phenotype is optimal for pollination success, i.e. fitness valleys are created. In such cases, plant species are expected to specialize on particular groups of flower visitors. Contrary to this expectation, it is commonly observed that flowers interact with various groups of visitors, while at the same time maintaining distinct phenotypes among ecotypes, subspecies, or congeners. This apparent paradox may be due to a gap in our understanding of how visitor-mediated trade-offs could affect floral adaptation. Here we provide a conceptual framework for analysing visitor-mediated trade-offs with the hope of stimulating empirical and theoretical studies to fill this gap. We propose two types of visitor-mediated trade-offs to address negative correlations among fitness contributions of different visitors: visitor-mediated phenotypic trade-offs (phenotypic trade-offs) and visitor-mediated opportunity trade-offs (opportunity trade-offs). Phenotypic trade-offs occur when different groups of visitors impose conflicting selection pressures on a floral trait. By contrast, opportunity trade-offs emerge only when some visitors’ actions (e.g. pollen collection) remove opportunities for fitness contribution by more beneficial visitors. Previous studies have observed disruptive selection due to phenotypic trade-offs less often than expected. In addition to existing explanations, we propose that some flowers have achieved ‘adaptive generalization’ by evolving features to avoid or eliminate the fitness valleys that phenotypic trade-offs tend to produce. The literature suggests a variety of pathways to such ‘trade-off mitigation’. Trade-off mitigation may also evolve as an adaptation to opportunity trade-offs. We argue that active exclusion, or floral specialization, can be viewed as a trade-off mitigation, occurring only when flowers cannot otherwise avoid strong opportunity trade-offs. These considerations suggest that an evolutionary strategy for trade-off mitigation is achieved often by acquiring novel combinations of traits. Thus, phenotypic diversification of flowers through convergent evolution of certain trait combinations may have been enhanced not only through adaptive specialization for particular visitors, but also through adaptive generalization for particular visitor communities. Explorations of how visitor-mediated trade-offs explain the recurrent patterns of floral phenotypes may help reconcile the long-lasting controversy on the validity of pollination syndromes.