Ecological bistability and evolutionary reversals under asymmetrical competition

Abstract How does the process of life‐history evolution interplay with population dynamics? Almost all models that have addressed this question assume that any combination of phenotypic traits uniquely determine the ecological population state. Here we show that if multiple ecological equilibria can exist, the evolution of a trait that relates to competitive performance can undergo adaptive reversals that drive cyclic alternation between population equilibria. The occurrence of evolutionary reversals requires neither environmentally driven changes in selective forces nor the coevolution of interactions with other species. The mechanism inducing evolutionary reversals is twofold. First, there exist phenotypes near which mutants can invade and yet fail to become fixed; although these mutants are eventually eliminated, their transitory growth causes the resident population to switch to an alternative ecological equilibrium. Second, asymmetrical competition causes the direction of selection to revert between high and low density. When ecological conditions for evolutionary reversals are not satisfied, the population evolves toward a steady state of either low or high abundance, depending on the degree of competitive asymmetry and environmental parameters. A sharp evolutionary transition between evolutionary stasis and evolutionary reversals and cycling can occur in response to a smooth change in ecological parameters, and this may have implications for our understanding of size‐abundance patterns.     

Traits related to species persistence and dispersal explain changes in plant communities subjected to habitat loss

Aim Habitat fragmentation is a major driver of biodiversity loss but it is insufficiently known how much its effects vary among species with different life‐history traits; especially in plant communities, the understanding of the role of traits related to species persistence and dispersal in determining dynamics of species communities in fragmented landscapes is still limited. The primary aim of this study was to test how plant traits related to persistence and dispersal and their interactions modify plant species vulnerability to decreasing habitat area and increasing isolation. Location Five regions distributed over four countries in Central and Northern Europe. Methods Our dataset was composed of primary data from studies on the distribution of plant communities in 300 grassland fragments in five regions. The regional datasets were consolidated by standardizing nomenclature and species life‐history traits and by recalculating standardized landscape measures from the original geographical data. We assessed the responses of plant species richness to habitat area, connectivity, plant life‐history traits and their interactions using linear mixed models. Results We found that the negative effect of habitat loss on plant species richness was pervasive across different regions, whereas the effect of habitat isolation on species richness was not evident. This area effect was, however, not equal for all the species, and life‐history traits related to both species persistence and dispersal modified plant sensitivity to habitat loss, indicating that both landscape and local processes determined large‐scale dynamics of plant communities. High competitive ability for light, annual life cycle and animal dispersal emerged as traits enabling species to cope with habitat loss. Main conclusions In highly fragmented rural landscapes in NW Europe, mitigating the spatial isolation of remaining grasslands should be accompanied by restoration measures aimed at improving habitat quality for low competitors, abiotically dispersed and perennial, clonal species.     

Wolf in sheep's clothing: Model misspecification undermines tests of the neutral theory for life histories

Understanding the processes behind change in reproductive state along life‐history trajectories is a salient research program in evolutionary ecology. Two processes, state dependence and heterogeneity, can drive the dynamics of change among states. Both processes can operate simultaneously, begging the difficult question of how to tease them apart in practice. The Neutral Theory for Life Histories (NTLH) holds that the bulk of variations in life‐history trajectories is due to state dependence and is hence neutral: Once previous (breeding) state is taken into account, variations are mostly random. Lifetime reproductive success (LRS), the number of descendants produced over an individual's reproductive life span, has been used to infer support for NTLH in natura. Support stemmed from accurate prediction of the population‐level distribution of LRS with parameters estimated from a state dependence model. We show with Monte Carlo simulations that the current reliance of NTLH on LRS prediction in a null hypothesis framework easily leads to selecting a misspecified model, biased estimates and flawed inferences. Support for the NTLH can be spurious because of a systematic positive bias in estimated state dependence when heterogeneity is present in the data but ignored in the analysis. This bias can lead to spurious positive covariance between fitness components when there is in fact an underlying trade‐off. Furthermore, neutrality implied by NTLH needs a clarification because of a probable disjunction between its common understanding by evolutionary ecologists and its translation into statistical models of life‐history trajectories. Irrespective of what neutrality entails, testing hypotheses about the dynamics of change among states in life histories requires a multimodel framework because state dependence and heterogeneity can easily be mistaken for each other.     

Contrasting patterns of density‐dependent selection at different life stages can create more than one fast–slow axis of life‐history variation

There has been much recent research interest in the existence of a major axis of life‐history variation along a fast–slow continuum within almost all major taxonomic groups. Eco‐evolutionary models of density‐dependent selection provide a general explanation for such observations of interspecific variation in the "pace of life." One issue, however, is that some large‐bodied long‐lived “slow” species (e.g., trees and large fish) often show an explosive “fast” type of reproduction with many small offspring, and species with “fast” adult life stages can have comparatively “slow” offspring life stages (e.g., mayflies). We attempt to explain such life‐history evolution using the same eco‐evolutionary modeling approach but with two life stages, separating adult reproductive strategies from offspring survival strategies. When the population dynamics in the two life stages are closely linked and affect each other, density‐dependent selection occurs in parallel on both reproduction and survival, producing the usual one‐dimensional fast–slow continuum (e.g., houseflies to blue whales). However, strong density dependence at either the adult reproduction or offspring survival life stage creates quasi‐independent population dynamics, allowing fast‐type reproduction alongside slow‐type survival (e.g., trees and large fish), or the perhaps rarer slow‐type reproduction alongside fast‐type survival (e.g., mayflies—short‐lived adults producing few long‐lived offspring). Therefore, most types of species life histories in nature can potentially be explained via the eco‐evolutionary consequences of density‐dependent selection given the possible separation of demographic effects at different life stages.     

Evolutionary and population dynamics of host–parasitoid interactions

The role of evolutionary dynamics in understanding host–parasitoid interactions is interlinked with the population dynamics of these interactions. Here, we address the problems in coupling evolutionary and population dynamics of host–parasitoid interactions. We review previous theoretical and empirical studies and show that evolution can alter the ecological dynamics of a host–parasitoid interaction. Whether evolution stabilizes or destabilizes the interaction depends on the direction of evolutionary changes, which are affected by ecological, physiological, and genetic details of the insect biology. We examine the effect of life history correlations on population persistence and stability, embedding two types, one of which is competitively inferior but superior in encapsulation (for parasitoid, virulence), in a Nicholson–Bailey model with intraspecific resource competition for host. If a trade-off exists between intraspecific competitive ability and encapsulation (or virulence, as a countermeasure) in both the host and parasitoid, the trade-off or even positive correlation in the parasitoid is less influential to ecological stability than the trade-off in the host. We comment on the bearing this work has on the broader issues of understanding host–parasitoid interactions, including long-term biological control. Received: November 10, 1998 / Accepted: January 18, 1999     

The interaction between plant competition and disease

It is well documented that pathogens can affect the survival, reproduction, and growth of individual plants. Drawing together insights from diverse studies in ecology and agriculture, we evaluate the evidence for pathogens affecting competitive interactions between plants of both the same and different species. Our objective is to explore the potential ecological and evolutionary consequences of such interactions. First, we address how disease interacts with intraspecific competition and present a simple graphical model suggesting that diverse outcomes should be expected. We conclude that the presence of pathogens may have either large or minimal effects on population dynamics depending on many factors including the density-dependent compensatory ability of healthy plants and spatial patterns of infection. Second, we consider how disease can alter competitive abilities of genotypes, and thus may affect the genetic composition of populations. These genetic processes feed back on population dynamics given trade-offs between disease resistance and other fitness components. Third, we examine how the effect of disease on interspecific plant interactions may have potentially far-reaching effects on community composition. A host-specific pathogen, for example, may alter a competitive hierarchy that exists between host and non-host species. Generalist pathogens can also induce indirect competitive interactions between host species. We conclude by highlighting lacunae in our current understanding and suggest that future studies should (1) examine a broader taxonomic range of pathogens since work to date has largely focused on fungal pathogens; (2) increase the use of field competition studies; (3) follow interactions for multiple generations; (4) characterize density-dependent processes; and (5) quantify pathogen, as well as plant, population and community dynamics.     

A process‐based metacommunity framework linking local and regional scale community ecology

The metacommunity concept has the potential to integrate local and regional dynamics within a general community ecology framework. To this end, the concept must move beyond the discrete archetypes that have largely defined it (e.g. neutral vs. species sorting) and better incorporate local scale species interactions and coexistence mechanisms. Here, we present a fundamental reconception of the framework that explicitly links local coexistence theory to the spatial processes inherent to metacommunity theory, allowing for a continuous range of competitive community dynamics. These dynamics emerge from the three underlying processes that shape ecological communities: (1) density‐independent responses to abiotic conditions, (2) density‐dependent biotic interactions and (3) dispersal. Stochasticity is incorporated in the demographic realisation of each of these processes. We formalise this framework using a simulation model that explores a wide range of competitive metacommunity dynamics by varying the strength of the underlying processes. Using this model and framework, we show how existing theories, including the traditional metacommunity archetypes, are linked by this common set of processes. We then use the model to generate new hypotheses about how the three processes combine to interactively shape diversity, functioning and stability within metacommunities.     

Individual heterogeneity in life histories and eco‐evolutionary dynamics

Individual heterogeneity in life history shapes eco‐evolutionary processes, and unobserved heterogeneity can affect demographic outputs characterising life history and population dynamical properties. Demographic frameworks like matrix models or integral projection models represent powerful approaches to disentangle mechanisms linking individual life histories and population‐level processes. Recent developments have provided important steps towards their application to study eco‐evolutionary dynamics, but so far individual heterogeneity has largely been ignored. Here, we present a general demographic framework that incorporates individual heterogeneity in a flexible way, by separating static and dynamic traits (discrete or continuous). First, we apply the framework to derive the consequences of ignoring heterogeneity for a range of widely used demographic outputs. A general conclusion is that besides the long‐term growth rate lambda, all parameters can be affected. Second, we discuss how the framework can help advance current demographic models of eco‐evolutionary dynamics, by incorporating individual heterogeneity. For both applications numerical examples are provided, including an empirical example for pike. For instance, we demonstrate that predicted demographic responses to climate warming can be reversed by increased heritability. We discuss how applications of this demographic framework incorporating individual heterogeneity can help answer key biological questions that require a detailed understanding of eco‐evolutionary dynamics.     

Condition‐dependent movement and dispersal in experimental metacommunities

Dispersal and the underlying movement behaviour are processes of pivotal importance for understanding and predicting metapopulation and metacommunity dynamics. Generally, dispersal decisions are condition‐dependent and rely on information in the broad sense, like the presence of conspecifics. However, studies on metacommunities that include interspecific interactions generally disregard condition‐dependence. Therefore, it remains unclear whether and how dispersal in metacommunities is condition‐dependent and whether rules derived from single‐species contexts can be scaled up to (meta)communities. Using experimental protist metacommunities, we show how dispersal and movement depend on and are adjusted by the strength of interspecific interactions. We found that the predicting movement and dispersal in metacommunities requires knowledge on behavioural responses to intra‐ and interspecific interaction strengths. Consequently, metacommunity dynamics inferred directly from single‐species metapopulations without taking interspecific interactions into account are likely flawed. Our work identifies the significance of condition‐dependence for understanding metacommunity dynamics, stability and the coexistence and distribution of species.     

Competition as a source of constraint on life history evolution in natural populations

Competition among individuals is central to our understanding of ecology and population dynamics. However, it could also have major implications for the evolution of resource-dependent life history traits (for example, growth, fecundity) that are important determinants of fitness in natural populations. This is because when competition occurs, the phenotype of each individual will be causally influenced by the phenotypes, and so the genotypes, of competitors. Theory tells us that indirect genetic effects arising from competitive interactions will give rise to the phenomenon of ‘evolutionary environmental deterioration'', and act as a source of evolutionary constraint on resource-dependent traits under natural selection. However, just how important this constraint is remains an unanswered question. This article seeks to stimulate empirical research in this area, first highlighting some patterns emerging from life history studies that are consistent with a competition-based model of evolutionary constraint, before describing several quantitative modelling strategies that could be usefully applied. A recurrent theme is that rigorous quantification of a competition''s impact on life history evolution will require an understanding of the causal pathways and behavioural processes by which genetic (co)variance structures arise. Knowledge of the G-matrix among life history traits is not, in and of itself, sufficient to identify the constraints caused by competition.     

What determines the relationship between plant diversity and habitat productivity?

The relationship between biodiversity and habitat productivity has been a fundamental topic in ecology. Although the relationship between these parameters may exhibit different shapes, the unimodal shape has been frequently encountered. The decrease in diversity at high productivity has usually been attributed to competitive exclusion. We suggest that evolutionary history and dispersal limitation may be even more important in shaping the diversity–productivity relationship. On a global scale, unimodal diversity–productivity relationships dominate in temperate regions, whereas positive relationships are more common in the tropics. This difference can be accounted for by contrasting evolutionary history. Temperate regions have smaller species pools for productive habitats since these habitats have been scarce historically for speciation, while the opposite is true for the tropics. In addition, dispersal within a region may limit diversity either due to the lack of dispersal syndromes at low productivity or the low number of diaspores at high productivity. Thereafter, biotic interactions (competition and facilitation) can shape the relationship. All these processes can act independently or concurrently. We recommend that the common approach to examining empirical diversity–environmental relationships should start with the role of large‐scale processes such as evolutionary history and dispersal limitation, followed by influences associated with ecological interactions.     

Plant life history and above–belowground interactions: missing links

The importance of above–belowground interactions for plant growth and community dynamics became clear in the last decades, whereas the numerous studies on plant life history improved our knowledge on eco‐evolutionary dynamics. However, surprisingly few studies have linked both research fields despite their potential to increase our mechanistic understanding of how above belowground interactions are governed. Here I briefly review studies on above–belowground interactions and plant life history and identify important research gaps. To advance our understanding of ecological strategies and eco‐evolutionary dynamics of plants and their associated organisms it is warranted to elucidate the interconnectivity and tradeoffs of plant life history traits of growth, defence, reproduction, nutrient cycling and the functional composition of above‐ and belowground heterotrophic communities. Using the concept of tradeoffs in growth, reproduction and defence we can postulate that plants in rich soil grow, reproduce and die fast whilst avoiding above‐ and belowground antagonists, whereas plants in poor soil grow slow, live and reproduce longer and invest in above‐ and belowground mutualists and defences. However, alternative scenarios are possible and depend on the selection pressure by above‐ and belowground mutualists and antagonists during plant ontogeny and via after‐life effects. To elucidate missing links between life history traits and above–belowground interactions, complementary modelling and empirical studies are needed that reveal the coupling between below‐ and aboveground plant traits of growth, defence and reproduction, their heritability and their cost/benefit relation. These cost/benefit analyses of defence should span from individuals to future generations, taking feedback effects via altered biotic communities and resource competition into account. The role of soil fertility in steering plant life history traits requires explicit testing of trans‐generational trait shifts in growth, defence, reproduction, cost/benefit of associations with mutualists and antagonists and soil feedbacks across plant genotypes/species with distinct life history traits, grown across soil fertility gradients.     

Impact of life stage specific immune priming on invertebrate disease dynamics

The immune response of a host can have important impacts on host‐pathogen interactions, but investment in immunity often changes dynamically across the life history of a host. One form of investment involves the induction of a primed immune response against previously encountered pathogens that protects the host from re‐infection. In addition to providing immediate protective effects, immune priming can also provide two types of ‘delayed’ protection against pathogens: priming across life stages (ontogenic priming) and priming across generations (trans‐generational priming). Consequently both types of immune priming have the potential to mediate life history variability in host–pathogen interactions, which could have important consequences for disease prevalence and dynamics as well as for the demographic structure of the host population. Here we develop a stage‐structured SIRS model for an invertebrate host to explore the relative and combined impact of ontogenic priming and trans‐generational priming on infection prevalence, host population size, and population age structure. Our model predicts that both types of immune priming can dramatically reduce disease prevalence at equilibrium, but their individual and combined effects on population size and age structure depend on the magnitude of tradeoffs between immune protection and reproduction as well as on the symmetry of infection parameters between life stages. This model underscores the potential importance of life‐history based immune investment patterns for disease dynamics and highlights the need for wide‐spread empirical estimation of parameters that represent the maintenance of immune priming in insects.     

Single‐ or multistage regulation in complex life cycles: does it make a difference?

Data on the different stages of complex life cycles are often rather unbalanced, especially those concerning the effects of density. How does this affect our understanding of a species’ population dynamics? Two discrete three‐stage models with overlapping generations and delayed maturation are constructed to address this question. They assume that survival or emigration in any life stage and/or reproduction can be density dependent. A typical pond‐breeding amphibian species with a well‐studied larval stage serves as an example. Numerical results show that the population dynamics resulting from density dependence at a single (e.g. the larval) stage can be decisively and unpredictably modified by density dependence in additional stages. Superposition of density‐dependent processes could thus be one reason for the difficulties in identifying density dependence in the field. Moreover, in a simulated source‐refuge system with habitat‐specific density‐dependent dispersal of juveniles density dependence in multiple stages can stabilize or destabilize the dynamics and produce misleading age structures. From an applied perspective this model shows that excluding multistage regulation prematurely clearly affects our ability to predict consequences of human impacts.     

A general model of local competition for space

Local competition for space across a wide array of taxa typically involves three mechanisms that we denote here as expansion (spreading into unoccupied habitat), lottery (replacing dead competitors), and overgrowth (encroaching on competitors along zones of contact). By formulating and analysing a simple, general model incorporating these features, we identify ecological conditions and life‐history features that lead to stable coexistence or competitive exclusion (with or without initial‐condition dependence) and gain insight by linking these to case studies in the literature. We demonstrate the importance of contact inhibition, a little‐studied feature of overgrowth, and we show how life‐history tradeoffs may influence and be influenced by local competition for space. The general model we present can help indicate whether local interactions are sufficient to explain patterns of coexistence or exclusion and can serve as the foundation for more specific, realistic models of spatial competition.     

Life history alterations upon oral and hemocoelic bacterial exposure in the butterfly Melitaea cinxia

Life history strategies often shape biological interactions by specifying the parameters for possible encounters, such as the timing, frequency, or way of exposure to parasites. Consequentially, alterations in life‐history strategies are closely intertwined with such interaction processes. Understanding the connection between life‐history alterations and host–parasite interactions can therefore be important to unveil potential links between adaptation to environmental change and changes in interaction processes. Here, we studied how two different host–parasite interaction processes, oral and hemocoelic exposure to bacteria, affect various life histories of the Glanville fritillary butterfly Melitaea cinxia. We either fed or injected adult butterflies with the bacterium Micrococcus luteus and observed for differences in immune defenses, reproductive life histories, and longevity, compared to control exposures. Our results indicate differences in how female butterflies adapt to the two exposure types. Orally infected females showed a reduction in clutch size and an earlier onset of reproduction, whereas a reduction in egg weight was observed for hemocoelically exposed females. Both exposure types also led to shorter intervals between clutches and a reduced life span. These results indicate a relationship between host–parasite interactions and changes in life‐history strategies. This relationship could cast restrictions on the ability to adapt to new environments and consequentially influence the population dynamics of a species in changing environmental conditions.     

Genetic diversity,virulence and fitness evolution in an obligate fungal parasite of bees

Within‐host competition is predicted to drive the evolution of virulence in parasites, but the precise outcomes of such interactions are often unpredictable due to many factors including the biology of the host and the parasite, stochastic events and co‐evolutionary interactions. Here, we use a serial passage experiment (SPE) with three strains of a heterothallic fungal parasite (Ascosphaera apis) of the Honey bee (Apis mellifera) to assess how evolving under increasing competitive pressure affects parasite virulence and fitness evolution. The results show an increase in virulence after successive generations of selection and consequently faster production of spores. This faster sporulation, however, did not translate into more spores being produced during this longer window of sporulation; rather, it appeared to induce a loss of fitness in terms of total spore production. There was no evidence to suggest that a greater diversity of competing strains was a driver of this increased virulence and subsequent fitness cost, but rather that strain‐specific competitive interactions influenced the evolutionary outcomes of mixed infections. It is possible that the parasite may have evolved to avoid competition with multiple strains because of its heterothallic mode of reproduction, which highlights the importance of understanding parasite biology when predicting disease dynamics.     

The effect of multi‐species host density on superparasitism and sex ratio in a gregarious parasitoid

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The genomic basis of eco‐evolutionary dynamics

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Frequency‐dependent and density‐dependent larval competition between life‐history strains of a fly,Lucilia cuprina

1. Competition was created between the larvae of two life‐history strains of the blowfly Lucilia cuprina (Wiedemann) that have different requirements for larval resource acquisition. Adult females of one strain had the ability to mature eggs in the absence of adult feeding (autogeny) whereas the other strain lacked this ability. Autogeny shifts the burden of resource acquisition from adults to larvae, potentially leading to greater competition at this earlier life history stage. 2. A replacement series was used to determine the per‐capita competitive effect between strains relative to the intra‐strain effect, and density‐ and frequency‐dependent variation in this per‐capita effect was then evaluated. Evidence was found of competitive superiority of autogenous larvae when they occurred at a low frequency and low density, but their competitive ability was lost or reversed at higher frequencies and densities. 3. A dynamic competitive environment created by frequency and density dependence can account for the maintenance of genetic diversity for major life‐history traits. Such competition may explain why autogeny is rare in field populations of L. cuprina even although underlying genetic variation for the trait seems to be present.