Travel costs, oviposition behaviour and the dynamics of insect–plant systems

Insect attack can have major consequences for plant population dynamics. We used individually based simulation models to ask how insect oviposition behaviour influences persistence and potential stability of an herbivore–plant system. We emphasised effects on system dynamics of herbivore travel costs and of two kinds of behaviour that might evolve to mitigate travel costs: insect clutch size behaviour (whether eggs are laid singly or in groups) and female aggregation behaviour (whether females prefer or avoid plants already bearing eggs). Travel costs that increase as plant populations drop lead to inverse density dependence of plant reproduction under herbivore attack. Female clutch size and aggregation behaviours also strongly affect system dynamics. When females lay eggs in large clutches or aggregate their clutches, herbivore damage varies strongly among plants, providing probabilistic refuges that permit plant reproduction and persistence. However, the population dynamics depend strongly on whether insect behaviour is fixed or responds adaptively to plant population size: when (and only when) females increase clutch size or aggregation as plants become rare, refuges from herbivory weaken at high plant density, creating inverse density dependence in plant reproduction. Both herbivore travel costs themselves, and also insect behaviour that might evolve in response to travel costs, can thus create plant density dependence—a basic requirement for regulation of plant populations by their insect herbivores.     

Can possible evolutionary outcomes be determined directly from the population dynamics?

Traditionally, to determine the possible evolutionary behaviour of an ecological system using adaptive dynamics, it is necessary to calculate the fitness and its derivatives at a singular point. We investigate the claim that the possible evolutionary behaviour can be predicted directly from the population dynamics, without the need for calculation, by applying three criteria — one based on the form of the density dependent rates and two on the role played by the evolving parameters. Taking a general continuous time model, with broad ecological range, we show that the claim is true. Initially, we assume that individuals enter in class 1 and move through population classes sequentially; later we relax these assumptions and find that the criteria still apply. However, when we consider models where the evolving parameters appear non-linearly in the dynamics, we find some aspects of the criteria fail; useful but weaker results on possible evolutionary behaviour now apply.     

Anomalous invasion dynamics due to dispersal polymorphism and dispersal–reproduction trade-offs

Dispersal polymorphism and mutation play significant roles during biological invasions, potentially leading to evolution and complex behaviour such as accelerating or decelerating invasion fronts. However, life-history theory predicts that reproductive fitness—another key determinant of invasion dynamics—may be lower for more dispersive strains. Here, we use a mathematical model to show that unexpected invasion dynamics emerge from the combination of heritable dispersal polymorphism, dispersal-fitness trade-offs, and mutation between strains. We show that the invasion dynamics are determined by the trade-off relationship between dispersal and population growth rates of the constituent strains. We find that invasion dynamics can be ‘anomalous’ (i.e. faster than any of the strains in isolation), but that the ultimate invasion speed is determined by the traits of, at most, two strains. The model is simple but generic, so we expect the predictions to apply to a wide range of ecological, evolutionary, or epidemiological invasions.     

The impact of cross-immunity, mutation and stochastic extinction on pathogen diversity

We examine the dynamics of antigenically diverse infectious agents using a mathematical model describing the transmission dynamics of arbitrary numbers of pathogen strains, interacting via cross-immunity, and in the presence of mutations generating new strains and stochastic extinctions of existing ones. Equilibrium dynamics fall into three classes depending on cross-immunity, transmissibility and host population size: systems where global extinction is likely, stable single-strain persistence, and multiple-strain persistence with stable diversity. Where multi-strain dynamics are stable, a diversity threshold region separates a low-prevalence, low-diversity region of parameter space from a high-diversity, high-prevalence region. The location of the threshold region is determined by the reproduction number of the pathogen and the intensity of cross-immunity, with the sharpness of the transition being determined by the manner in which immunity accrues with repeated infections. Host population size and cross-immunity are found to be the most decisive factors in determining pathogen diversity. While the model framework developed is simplified, we show that it can capture essential aspects of the complex evolutionary dynamics of pathogens such as influenza.     

Can possible evolutionary outcomes be determined directly from the population dynamics?

Traditionally, to determine the possible evolutionary behaviour of an ecological system using adaptive dynamics, it is necessary to calculate the fitness and its derivatives at a singular point. We investigate the claim that the possible evolutionary behaviour can be predicted directly from the population dynamics, without the need for calculation, by applying three criteria — one based on the form of the density dependent rates and two on the role played by the evolving parameters. Taking a general continuous time model, with broad ecological range, we show that the claim is true. Initially, we assume that individuals enter in class 1 and move through population classes sequentially; later we relax these assumptions and find that the criteria still apply. However, when we consider models where the evolving parameters appear non-linearly in the dynamics, we find some aspects of the criteria fail; useful but weaker results on possible evolutionary behaviour now apply.     

A long winter for the Red Queen: rethinking the evolution of seasonal migration

This paper advances an hypothesis that the primary adaptive driver of seasonal migration is maintenance of site fidelity to familiar breeding locations. We argue that seasonal migration is therefore principally an adaptation for geographic persistence when confronted with seasonality – analogous to hibernation, freeze tolerance, or other organismal adaptations to cyclically fluctuating environments. These ideas stand in contrast to traditional views that bird migration evolved as an adaptive dispersal strategy for exploiting new breeding areas and avoiding competitors. Our synthesis is supported by a large body of research on avian breeding biology that demonstrates the reproductive benefits of breeding‐site fidelity. Conceptualizing migration as an adaptation for persistence places new emphasis on understanding the evolutionary trade‐offs between migratory behaviour and other adaptations to fluctuating environments both within and across species. Seasonality‐induced departures from breeding areas, coupled with the reproductive benefits of maintaining breeding‐site fidelity, also provide a mechanism for explaining the evolution of migration that is agnostic to the geographic origin of migratory lineages (i.e. temperate or tropical). Thus, our framework reconciles much of the conflict in previous research on the historical biogeography of migratory species. Although migratory behaviour and geographic range change fluidly and rapidly in many populations, we argue that the loss of plasticity for migration via canalization is an overlooked aspect of the evolutionary dynamics of migration and helps explain the idiosyncratic distributions and migratory routes of long‐distance migrants. Our synthesis, which revolves around the insight that migratory organisms travel long distances simply to stay in the same place, provides a necessary evolutionary context for understanding historical biogeographic patterns in migratory lineages as well as the ecological dynamics of migratory connectivity between breeding and non‐breeding locations.     

Stochasticity generates an evolutionary instability for infectious disease

Traditional models of disease evolution are based upon the deterministic competition between strains that confer complete cross-immunity, and predict the selection of strains with higher basic reproductive ratios ( R ₀). In contrast, evolution in a stochastic setting is determined by a complex mixture of influences. Here, to isolate the impact of stochasticity, we constrain all competing strains to have an equal basic reproductive ratio – thereby eliminating deterministic selection. The resulting stochastic models predict an evolutionary unstable strategy, which separates a region favouring the evolution of rapid-transmission (acute) strains from one favouring persistent (chronic) strains. We find this to be a generic phenomenon with strain evolution consistently driven towards extremes of epidemiological behaviour. Even in the absence of an equal R ₀ constraint, such stochastic selective pressures operate in addition to standard deterministic selection and will therefore influence the evolutionary behaviour of disease in all scenarios.     

Evolutionary implications for interactions between multiple strains of host and parasite

The interaction between multiple parasite strains within different host types may influence the evolutionary trajectories of parasites. In this article, we formulate a deterministic model with two strains of parasites and two host types in order to investigate how heterogeneities in parasite virulence and host life-history may affect the persistence and spread of diseases in natural systems. We compute the reproductive number of strain i (R(i)) independently, as well as the (conditional) "invasion" reproductive number for strains i (R(i)(j), j not equal i) when strain j is at a positive equilibrium. We show that the disease-free equilibrium is locally asymptotically stable if R(i)<1 for both strains and is unstable if R(i)>1 for one stain. We establish the criterion R(i)(j)>1 for strain i to invade strain j. Subthreshold coexistence driven by coinfection is possible even when R(i) of one strain is below 1. We identify conditions that determine the evolution of parasite specialism or generalism based on the life-history strategies employed by hosts, and investigate how host strains may influence parasite persistence.     

Trade-offs between and within scales: environmental persistence and within-host fitness of avian influenza viruses

Trade-offs between different components of a pathogen''s replication and transmission cycle are thought to be common. A number of studies have identified trade-offs that emerge across scales, reflecting the tension between strategies that optimize within-host proliferation and large-scale population spread. Most of these studies are theoretical in nature, with direct experimental tests of such cross-scale trade-offs still rare. Here, we report an analysis of avian influenza A viruses across scales, focusing on the phenotype of temperature-dependent viral persistence. Taking advantage of a unique dataset that reports both environmental virus decay rates and strain-specific viral kinetics from duck challenge experiments, we show that the temperature-dependent environmental decay rate of a strain does not impact within-host virus load. Hence, for this phenotype, the scales of within-host infection dynamics and between-host environmental persistence do not seem to interact: viral fitness may be optimized on each scale without cross-scale trade-offs. Instead, we confirm the existence of a temperature-dependent persistence trade-off on a single scale, with some strains favouring environmental persistence in water at low temperatures while others reduce sensitivity to increasing temperatures. We show that this temperature-dependent trade-off is a robust phenomenon and does not depend on the details of data analysis. Our findings suggest that viruses might employ different environmental persistence strategies, which facilitates the coexistence of diverse strains in ecological niches. We conclude that a better understanding of the transmission and evolutionary dynamics of influenza A viruses probably requires empirical information regarding both within-host dynamics and environmental traits, integrated within a combined ecological and within-host framework.     

Persistence and resistance as complementary bacterial adaptations to antibiotics

Bacterial persistence represents a simple of phenotypic heterogeneity, whereby a proportion of cells in an isogenic bacterial population can survive exposure to lethal stresses such as antibiotics. In contrast, genetically based antibiotic resistance allows for continued growth in the presence of antibiotics. It is unclear, however, whether resistance and persistence are complementary or alternative evolutionary adaptations to antibiotics. Here, we investigate the co‐evolution of resistance and persistence across the genus Pseudomonas using comparative methods that correct for phylogenetic nonindependence. We find that strains of Pseudomonas vary extensively in both their intrinsic resistance to antibiotics (ciprofloxacin and rifampicin) and persistence following exposure to these antibiotics. Crucially, we find that persistence correlates positively to antibiotic resistance across strains. However, we find that different genes control resistance and persistence implying that they are independent traits. Specifically, we find that the number of type II toxin–antitoxin systems (TAs) in the genome of a strain is correlated to persistence, but not resistance. Our study shows that persistence and antibiotic resistance are complementary, but independent, evolutionary adaptations to stress and it highlights the key role played by TAs in the evolution of persistence.     

Colonization and persistence ability explain the extent to which plant species fill their potential range

Aim How species traits and environmental conditions affect biogeographical dynamics is poorly understood. Here we test whether estimates of a species’ evolutionary age, colonization and persistence ability can explain its current ‘range filling’ (the ratio between realized and potential range size). Location Fynbos biome (Cape Floristic Region, South Africa). Methods For 37 species of woody plants (Proteaceae), we estimate range filling using atlas data and distribution models, evolutionary age using molecular phylogenies, and persistence ability using estimates of individual longevity (which determines the probability of extinction of local populations). Colonization ability is estimated from validated process‐based seed dispersal models, the arrangement of potential habitat, and data on local abundance. To relate interspecific variation in range filling to evolutionary age, colonization and persistence ability, we use two complementary model types: phenomenological linear models and the process‐based metapopulation model of Levins. Results Linear model analyses show that range filling increases with a species’ colonization and persistence ability but is not affected by species age. Moreover, colonization ability is a better predictor of range filling than its component variables (local abundance and dispersal ability). The phylogenetically independent interaction between colonization and persistence ability is significant (P < 0.05) for 97% of 180 alternative phylogenies. While the selected linear model explains 42% of the variance in arcsine transformed range filling, the Levins model performs more poorly. It overestimates range filling for realistic parameter values and produces unrealistic parameter estimates when fitted statistically. Main conclusions Colonization and local extinction seem to shape Proteaceae range dynamics on ecological rather than macroevolutionary time‐scales. Our results suggest that the positive abundance–range size relationship in this group is due primarily to the effect of abundance on colonization. In summary, this study contributes to a process‐based understanding of range dynamics and highlights the importance of colonization for the future survival of Fynbos Proteaceae.     

How the type of anthropogenic change alters the consequences of ecological traps

Understanding altered ecological and evolutionary dynamics in novel environments is vital for predicting species responses to rapid environmental change. One fundamental concept relevant to such dynamics is the ecological trap, which arises from rapid anthropogenic change and can facilitate extinction. Ecological traps occur when formerly adaptive habitat preferences become maladaptive because the cues individuals preferentially use in selecting habitats lead to lower fitness than other alternatives. While it has been emphasized that traps can arise from different types of anthropogenic change, the resulting consequences of these different types of traps remain unknown. Using a novel model framework that builds upon the Price equation from evolutionary genetics, we provide the first analysis that contrasts the ecological and evolutionary consequences of ecological traps arising from two general types of perturbations known to trigger traps. Our model suggests that traps arising from degradation of existing habitats are more likely to facilitate extinction than those arising from the addition of novel trap habitat. Importantly, our framework reveals the mechanisms of these outcomes and the substantial scope for persistence via rapid evolution that may buffer many populations from extinction, helping to resolve the paradox of continued persistence of many species in dramatically altered landscapes.     

Evolution of complex dynamics in spatially structured populations

Dynamics of populations depend on demographic parameters which may change during evolution. In simple ecological models given by one-dimensional difference equations, the evolution of demographic parameters generally leads to equilibrium population dynamics. Here we show that this is not true in spatially structured ecological models. Using a multi-patch metapopulation model, we study the evolutionary dynamics of phenotypes that differ both in their response to local crowding, i.e. in their competitive behaviour within a habitat, and in their rate of dispersal between habitats. Our simulation results show that evolution can favour phenotypes that have the intrinsic potential for very complex dynamics provided that the environment is spatially structured and temporally variable. These phenotypes owe their evolutionary persistence to their large dispersal rates. They typically coexist with phenotypes that have low dispersal rates and that exhibit equilibrium dynamics when alone. This coexistence is brought about through the phenomenon of evolutionary branching, during which an initially uniform population splits into the two phenotypic classes.     

Population Bottlenecks Strongly Affect the Evolutionary Dynamics of Antibiotic Persistence

Bacterial persistence is a potential cause of antibiotic therapy failure. Antibiotic-tolerant persisters originate from phenotypic differentiation within a susceptible population, occurring with a frequency that can be altered by mutations. Recent studies have proven that persistence is a highly evolvable trait and, consequently, an important evolutionary strategy of bacterial populations to adapt to high-dose antibiotic therapy. Yet, the factors that govern the evolutionary dynamics of persistence are currently poorly understood. Theoretical studies predict far-reaching effects of bottlenecking on the evolutionary adaption of bacterial populations, but these effects have never been investigated in the context of persistence. Bottlenecking events are frequently encountered by infecting pathogens during host-to-host transmission and antibiotic treatment. In this study, we used a combination of experimental evolution and barcoded knockout libraries to examine how population bottlenecking affects the evolutionary dynamics of persistence. In accordance with existing hypotheses, small bottlenecks were found to restrict the adaptive potential of populations and result in more heterogeneous evolutionary outcomes. Evolutionary trajectories followed in small-bottlenecking regimes additionally suggest that the fitness landscape associated with persistence has a rugged topography, with distinct trajectories toward increased persistence that are accessible to evolving populations. Furthermore, sequencing data of evolved populations and knockout libraries after selection reveal various genes that are potentially involved in persistence, including previously known as well as novel targets. Together, our results do not only provide experimental evidence for evolutionary theories, but also contribute to a better understanding of the environmental and genetic factors that guide bacterial adaptation to antibiotic treatment.     

Behaviourally structured populations persist longer under harsh environmental conditions

The factors and mechanisms that enhance population persistence in a fragmented habitat and/or under harsh environmental conditions are of significant current interest. We consider the dynamics of a population in an isolated habitat surrounded by an unfavourable environment subject to different behavioural responses between the individuals. We assume that there are two responses available: one of them is aggression in its extreme form, the other is its contrary when an individual takes flight in order to avoid any contact with its conspecific. We show that a behaviourally structured population consisting of individuals with fixed behavioural responses is intrinsically less prone to extinction under harsh environmental condition than a population where the individuals can ‘choose’ between the two given behaviours. We also show that, contrary to an intuitively expected negative impact of aggression on population persistence, the optimal conditions for population persistence are reached when a considerable proportion of the individuals exhibit aggressive behaviour.     

Serotype cycles in cholera dynamics

Interest in understanding strain diversity and its impact on disease dynamics has grown over the past decade. Theoretical disease models of several co-circulating strains indicate that incomplete cross-immunity generates conditions for strain-cycling behaviour at the population level. However, there have been no quantitative analyses of disease time-series that are clear examples of theoretically expected strain cycling. Here, we analyse a 40-year (1966-2005) cholera time-series from Bangladesh to determine whether patterns evident in these data are compatible with serotype-cycling behaviour. A mathematical two-serotype model is capable of explaining the oscillations in case patterns when cross-immunity between the two serotypes, Inaba and Ogawa, is high. Further support that cholera's serotype-cycling arises from population-level immunity patterns is provided by calculations of time-varying effective reproductive rates. These results shed light on historically observed serotype dominance shifts and have important implications for cholera early warning systems.     

Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia

Mutualistic interactions are widespread and obligatory for manyorganisms, yet their evolutionary persistence in the face ofcheating is theoretically puzzling. Nutrient-acquisition symbiosesbetween plants and soil microbes are critically important toplant evolution and ecosystem function, yet we know almost nothingabout the evolutionary dynamics and mechanisms of persistenceof these ancient mutualisms. Partner-choice and partner-fidelityare mechanisms for dealing with cheaters, and can theoreticallyallow mutualisms to persist despite cheaters. Many models of cooperative behavior assume pairwise interactions,while most plant-microbe nutrient-acquisition symbioses involvea single plant interacting with numerous microbes. Market models,in contrast, are well suited to mutualisms in which single plantsattempt to conduct mutually beneficial resource exchange withmultiple individuals. Market models assume that one partnerchooses to trade with a subset of individuals selected froma market of potential partners. Hence, determining whether partner-choiceoccurs in plant-microbe mutualisms is critical to understandingthe evolutionary persistence and dynamics of these symbioses.The nitrogen-fixation/carbon-fixation mutualism between leguminousplants and rhizobial bacteria is widespread, ancient, and importantfor ecosystem function and human nutrition. It also involvessingle plants interacting simultaneously with several to manybacterial partners, including ineffective ("cheating") strains.We review the existing literature and find that this mutualismdisplays several elements of partner-choice, and may match therequirements of the market paradigm. We conclude by identifyingprofitable questions for future research.     

On the importance of evolving phenotype distributions on evolutionary diversification

Evolutionary branching occurs when a population with a unimodal phenotype distribution diversifies into a multimodally distributed population consisting of two or more strains. Branching results from frequency-dependent selection, which is caused by interactions between individuals. For example, a population performing a social task may diversify into a cooperator strain and a defector strain. Branching can also occur in multi-dimensional phenotype spaces, such as when two tasks are performed simultaneously. In such cases, the strains may diverge in different directions: possible outcomes include division of labor (with each population performing one of the tasks) or the diversification into a strain that performs both tasks and another that performs neither. Here we show that the shape of the population’s phenotypic distribution plays a role in determining the direction of branching. Furthermore, we show that the shape of the distribution is, in turn, contingent on the direction of approach to the evolutionary branching point. This results in a distribution–selection feedback that is not captured in analytical models of evolutionary branching, which assume monomorphic populations. Finally, we show that this feedback can influence long-term evolutionary dynamics and promote the evolution of division of labor.     

A Multi-scale Analysis of Influenza A Virus Fitness Trade-offs due to Temperature-dependent Virus Persistence

Successful replication within an infected host and successful transmission between hosts are key to the continued spread of most pathogens. Competing selection pressures exerted at these different scales can lead to evolutionary trade-offs between the determinants of fitness within and between hosts. Here, we examine such a trade-off in the context of influenza A viruses and the differential pressures exerted by temperature-dependent virus persistence. For a panel of avian influenza A virus strains, we find evidence for a trade-off between the persistence at high versus low temperatures. Combining a within-host model of influenza infection dynamics with a between-host transmission model, we study how such a trade-off affects virus fitness on the host population level. We show that conclusions regarding overall fitness are affected by the type of link assumed between the within- and between-host levels and the main route of transmission (direct or environmental). The relative importance of virulence and immune response mediated virus clearance are also found to influence the fitness impacts of virus persistence at low versus high temperatures. Based on our results, we predict that if transmission occurs mainly directly and scales linearly with virus load, and virulence or immune responses are negligible, the evolutionary pressure for influenza viruses to evolve toward good persistence at high within-host temperatures dominates. For all other scenarios, influenza viruses with good environmental persistence at low temperatures seem to be favored.