Co-evolution as an important component explaining microbial predator-prey interaction.

Predator-prey relationships belong to the most important and well-studied ecological interactions in nature. Understanding the underlying mechanisms is important to predict community dynamics and to estimate coexistence probability. Historically, evolution has been considered to be too slow to affect such ecological interactions. However, evolution can occur within ecological time scales, potentially affecting predator-prey communities. In an antagonistic pair-wise relationship the prey might evolve to minimize the effect caused by the predator (e.g. mortality), while the predator might evolve to maximize the effect (e.g. food intake). Evolution of one of the species or even co-evolution of both species in predator-prey relationships is often difficult to estimate from population dynamics without measuring of trait changes in predator and/or prey population. Particularly in microbial systems, where microorganisms evolve quickly, determining whether co-evolution occurs in predator-prey systems is challenging. We simulate observational data using quantitative trait evolution models and show that the interaction between bacteria and ciliates can be best explained as a co-evolutionary process, where both the prey and predator evolve. Evolution by prey alone explains the data less well, whereas the models with predator evolution alone or no evolution are both failing. We conclude that that ecology and evolution both interact in shaping community dynamics in microcosms. Ignoring the contribution of evolution might lead to incorrect conclusions.

Outside-host phage therapy as a biological control against environmental infectious diseases.

BACKGROUND: Environmentally growing pathogens present an increasing threat for human health, wildlife and food production. Treating the hosts with antibiotics or parasitic bacteriophages fail to eliminate diseases that grow also in the outside-host environment. However, bacteriophages could be utilized to suppress the pathogen population sizes in the outside-host environment in order to prevent disease outbreaks. Here, we introduce a novel epidemiological model to assess how the phage infections of the bacterial pathogens affect epidemiological dynamics of the environmentally growing pathogens. We assess whether the phage therapy in the outside-host environment could be utilized as a biological control method against these diseases. We also consider how phage-resistant competitors affect the outcome, a common problem in phage therapy. The models give predictions for the scenarios where the outside-host phage therapy will work and where it will fail to control the disease. Parameterization of the model is based on the fish columnaris disease that causes significant economic losses to aquaculture worldwide. However, the model is also suitable for other environmentally growing bacterial diseases. RESULTS: Transmission rates of the phage determine the success of infectious disease control, with high-transmission phage enabling the recovery of the host population that would in the absence of the phage go asymptotically extinct due to the disease. In the presence of outside-host bacterial competition between the pathogen and phage-resistant strain, the trade-off between the pathogen infectivity and the phage resistance determines phage therapy outcome from stable coexistence to local host extinction. CONCLUSIONS: We propose that the success of phage therapy strongly depends on the underlying biology, such as the strength of trade-off between the pathogen infectivity and the phage-resistance, as well as on the rate that the phages infect the bacteria. Our results indicate that phage therapy can fail if there are phage-resistant bacteria and the trade-off between pathogen infectivity and phage resistance does not completely inhibit the pathogen infectivity. Also, the rate that the phages infect the bacteria should be sufficiently high for phage-therapy to succeed.

Evolutionary contribution to coexistence of competitors in microbial food webs.

The theory of species coexistence is a key concept in ecology that has received much attention. The role of rapid evolution for determining species coexistence is still poorly understood although evolutionary change on ecological time-scales has the potential to change almost any ecological process. The influence of evolution on coexistence can be especially pronounced in microbial communities where organisms often have large population sizes and short generation times. Previous work on coexistence has assumed that traits involved in resource use and species interactions are constant or change very slowly in terms of ecological time-scales. However, recent work suggests that these traits can evolve rapidly. Nevertheless, the importance of rapid evolution to coexistence has not been tested experimentally. Here, we show how rapid evolution alters the frequency of two bacterial competitors over time when grown together with specialist consumers (bacteriophages), a generalist consumer (protozoan) and all in combination. We find that consumers facilitate coexistence in a manner consistent with classic ecological theory. However, through disentangling the relative contributions of ecology (changes in consumer abundance) and evolution (changes in traits mediating species interactions) on the frequency of the two competitors over time, we find differences between the consumer types and combinations. Overall, our results indicate that the influence of evolution on species coexistence strongly depends on the traits and species interactions considered.

Host Resistance and Behavior Determine Invasion Dynamics of a Detrimental Aquatic Disease.

Understanding the role of variation in host resistance and the multitude of transmission modes of parasites infecting hosts with complex behavioral interactions is essential for the control of emerging diseases. We used a discrete stage model to study the invasion dynamics of crayfish plague-an example of a detrimental disease-into a naïve host population that displays within-population variation in resistance of environmental infections and juvenile classes that are safe from contacts with adults. In the model, infection sources include four age classes of crayfish, contaminated carcasses, and free-dwelling zoospores. Disease transmission occurs via environment with a threshold infection density and through contacts, cannibalism, and scavenging of disease-killed conspecifics. Even if the infection is fatal, coexistence of the host and the parasite can be facilitated by variance of resistance and survival of the hiding juveniles. The model can be applied in the control of emerging diseases especially in crayfish-like organisms.

Impact of climate change and prey abundance on nesting success of a top predator, the goshawk.

Contemporary research has documented a large number of shifts in spring phenology and changes in distribution range although the average spring temperatures have increased by only 0.3-0.6 °C over the past 100 years. Generally, earlier breeding birds have larger clutch sizes, and the advancing spring could thus potentially increase breeding success. Shifts in spring phenology can, however, be crucial for bird reproduction, and mistiming the breeding event may even have negative consequences for population development. Our aim was to explore how weather and prey abundance relates to the breeding performance of a north European top predator, the northern goshawk Accipiter gentilis. Our nationwide dataset from Finland, spanning the period 1989-2004, shows that ambient weather has a greater impact on the timing and success of breeding than the density of grouse Tetraonidae, the main prey of goshawks. Higher early spring temperatures were associated with advancing hatching date of goshawks. Correspondingly, grouse density and temperature during laying and brooding were positively associated with brood size, while precipitation showed a negative connection. Applying our models to a future scenario of climate warming, combined with a 50 % reduction in grouse density, suggests that average breeding dates will advance only 2.5 days and average breeding success would remain the same. Notably, breeding success was not spatially equal throughout Finland, as northern and eastern populations suffered most from declining grouse densities. The observed pattern is thus the opposite to what is expected from a population situated at the northern edge of its distribution range, and thus may help to understand why populations may not increase at the northern edge of their thermal distribution due to climate change.

Crayfish population size under different routes of pathogen transmission.

We present an epidemiological model for the crayfish plague, a disease caused by an invasive oomycete Aphanomyces astaci, and its general susceptible freshwater crayfish host. The pathogen shows high virulence with resulting high mortality rates in freshwater crayfishes native to Europe, Asia, Australia, and South America. The crayfish plague occurrence shows complicated dynamics due to the several types of possible infection routes, which include cannibalism and necrophagy. We explore this complexity by addressing the roles of host cannibalism and the multiple routes of transmission through (1) environment, (2) contact, (3) cannibalism, and (4) scavenging of infected carcasses. We describe a compartment model having six classes of crayfish and a pool of crayfish plague spores from a single nonevolving strain. We show that environmental transmission is the decisive factor in the development of epidemics. Compared with a pathogen-free crayfish population, the presence of the pathogen with a low environmental transmission rate, regardless of the contact transmission rate, decreases the crayfish population size with a low risk of extinction. Conversely, a high transmission rate could drive both the crayfish and pathogen populations to extinction. High contact transmission rate with a low but nonzero environmental transmission rate can have mixed outcomes from extinction to large healthy population, depending on the initial values. Scavenging and cannibalism have a relevant role only when the environmental transmission rate is low, but scavenging can destabilize the system by transmitting the pathogen from a dead to a susceptible host. To the contrary, cannibalism stabilizes the dynamics by decreasing the proportion of infected population. Our model provides a simple tool for further analysis of complex host parasite dynamics and for the general understanding of crayfish disease dynamics in the wild.

Species dynamics alter community diversity-biomass stability relationships.

The relationship between community diversity and biomass variability remains a crucial ecological topic, with positive, negative and neutral diversity-stability relationships reported from empirical studies. Theory highlights the relative importance of Species-Species or Species-Environment interactions in driving diversity-stability patterns. Much previous work is based on an assumption of identical (stable) species-level dynamics. We studied ecosystem models incorporating stable, cyclic and more complex species-level dynamics, with either linear or non-linear density dependence, within a locally stable community framework. Species composition varies with increasing diversity, interacting with the correlation of species' environmental responses to drive either positive or negative diversity-stability patterns, which theory based on communities with only stable species-level dynamics fails to predict. Including different dynamics points to new mechanisms that drive the full range of diversity-biomass stability relationships in empirical systems where a wider range of dynamical behaviours are important.

The effect of dilution on eco-evolutionary dynamics of experimental microbial communities.

Changing environmental conditions can infer structural modifications of predator-prey communities. New conditions often increase mortality which reduces population sizes. Following this, predation pressure may decrease until populations are dense again. Dilution may thus have substantial impact not only on ecological but also on evolutionary dynamics because it amends population densities. Experimental studies, in which microbial populations are maintained by a repeated dilution into fresh conditions after a certain period, are extensively used approaches allowing us to obtain mechanistic insights into fundamental processes. By design, dilution, which depends on transfer volume (modifying mortality) and transfer interval (determining the time of interaction), is an inherent feature of these experiments, but often receives little attention. We further explore previously published data from a live predator-prey (bacteria and ciliates) system which investigated eco-evolutionary principles and apply a mathematical model to predict how various transfer volumes and transfer intervals would affect such an experiment. We find not only the ecological dynamics to be modified by both factors but also the evolutionary rates to be affected. Our work predicts that the evolution of the anti-predator defense in the bacteria, and the evolution of the predation efficiency in the ciliates, both slow down with lower transfer volume, but speed up with longer transfer intervals. Our results provide testable hypotheses for future studies of predator-prey systems, and we hope this work will help improve our understanding of how ecological and evolutionary processes together shape composition of microbial communities.

Infective prey leads to a partial role reversal in a predator-prey interaction.

An infective prey has the potential to infect, kill and consume its predator. Such a prey-predator relationship fundamentally differs from the predator-prey interaction because the prey can directly profit from the predator as a growth resource. Here we present a population dynamics model of partial role reversal in the predator-prey interaction of two species, the bottom dwelling marine deposit feeder sea cucumber Apostichopus japonicus and an important food source for the sea cucumber but potentially infective bacterium Vibrio splendidus. We analyse the effects of different parameters, e.g. infectivity and grazing rate, on the population sizes. We show that relative population sizes of the sea cucumber and V. Splendidus may switch with increasing infectivity. We also show that in the partial role reversal interaction the infective prey may benefit from the presence of the predator such that the population size may exceed the value of the carrying capacity of the prey in the absence of the predator. We also analysed the conditions for species extinction. The extinction of the prey, V. splendidus, may occur when its growth rate is low, or in the absence of infectivity. The extinction of the predator, A. japonicus, may follow if either the infectivity of the prey is high or a moderately infective prey is abundant. We conclude that partial role reversal is an undervalued subject in predator-prey studies.

The effects of functional response and host abundance fluctuations on genetic rescue in parasitoids with single-locus sex determination.

Many parasitoids have single-locus complementary sex determination (sl-CSD), which produces sterile or inviable males when homozygous at the sex determining locus. A previous study theoretically showed that small populations have elevated risks of extinction due to the positive feedback between inbreeding and small population size, referred to as the diploid male vortex. A few modeling studies have suggested that the diploid male vortex may not be as common because balancing selection at sex determining loci tends to maintain high allelic diversity in spatially structured populations. However, the generality of the conclusion is yet uncertain, as they were drawn either from models developed for particular systems or from a general-purpose competition model. To attest the conclusion, we study several well-studied host-parasitoid models that incorporate functional response specifying the number of attacked hosts given a host density and derive the conditions for a diploid male vortex in a single population. Then, we develop spatially structured individual-based versions of the models to include female behavior, diploid male fertility, and temporal fluctuations. The results show that producing a handful of successful offspring per female parasitoid could enable parasitoid persistence when a typical number of CSD alleles are present. The effect of functional response depends on the levels of fluctuations in host abundance, and inviable or partially fertile diploid males and a small increase in dispersal can alleviate the risk of a diploid male vortex. Our work supports the generality of effective genetic rescue in spatially connected parasitoid populations with sl-CSD. However, under more variable climate, the efficacy of the CSD mechanism may substantially decline.

When can we distinguish between neutral and non-neutral processes in community dynamics under ecological drift?

Determining whether the composition of ecological communities (species presence and abundance), can be predicted from species demographic traits, rather than being a result of neutral drift, is a key ecological question. Here we compare the similarity of community composition, from different community assembly models run under identical environmental conditions, where interspecific competition is assumed to be either neutral or niche-based. In both cases, species colonize a focal patch from a network of neighbouring patches in a metacommunity. We highlight the circumstances (rate and spatial scale of dispersal, and the relative importance of ecological drift) where commonly used community similarity metrics or species rank-abundance relationships are likely to give similar results, regardless of the underlying processes (neutral or non-neural) driving species' dynamics. As drift becomes more important in driving species abundances, deterministic niche structure has a smaller influence. Our ability to discriminate between different underlying processes driving community organization depends on the relative importance of different drift processes that operate on different spatial scales.

Seasonal clines of evolutionarily stable reproductive effort in insects.

For ectotherms, growth and reproduction are possible only during a limited period of the year in seasonal environments. In insects, fitness is generally maximized by producing as many generations as possible within a season, and in many species, the number of generations produced (voltinism) increases with increasing season length. In this study, we analyzed variation in adult life histories in insects along a climatic gradient. The analyzed trait is reproductive effort (resource allocation to reproduction). We begin by formalizing the trade-off between current reproduction and subsequent survival generated by reproductive effort. It appeared that reproductive effort is correlated positively with early fecundity and negatively with lifetime fecundity and life span. Then, deriving from that trade-off, we analyze the evolutionary stability of different schedules of age-specific fecundity that are generated by divergent reproductive effort. The analysis was carried out in season lengths that promote either univoltine or bivoltine phenology. The evolutionarily stable reproductive effort decreases with increasing season length in both phenologies, with a sudden increase when a change from univoltine to partially bivoltine phenology takes place. Reproductive effort responds strongly to changing phenology when density-dependent mortality occurs during diapause and weakly when juvenile mortality is density dependent.

Community stability under different correlation structures of species' environmental responses.

The outcome of species interactions in a variable environment is expected to depend on how similarly different species react to variation in environmental conditions. We study community stability (evenness and species diversity) in competitive communities that are either closed or subjected to random migration, under different regimes of environmental forcing. Community members respond to environmental variation: (i) independently (IR), (ii) in a positively correlated way (CR), or (iii) hierarchically, according to niche differences (HR). Increasing the amplitude of environmental variation and environmental reddening both reduce species evenness in closed communities through a reduction in species richness and increased skew in species abundances, under all three environmental response scenarios, although autocorrelation only has a minor effect with HR. Open communities show important qualitative differences, according to changes in the correlation structure of species' environmental responses. There is an intermediate minimum in evenness for HR communities with increasing environmental amplitude, explained by the interaction of changes in species richness and changes in the variance of within-species environmental responses across the community. Changes in autocorrelation also lead to qualitative differences between IR, CR and HR communities. Our results highlight the importance of considering mechanistically derived, hierarchical environmental correlations between species when addressing the influence of environmental variation on ecological communities, not only uniform environmental correlation across all species within a community.

Interactions between ecological traits and host plant type explain distribution change in noctuid moths.

The ecological traits of species determine how well a species can withstand threats to which it is exposed. If these predisposing traits can be identified, species that are most at risk of decline can be identified and an understanding of the processes behind the declines can be gained. We sought to determine how body size, specificity of larval host plant, overwintering stage, type of host plant, and the interactions of these traits are related to the distribution change in noctuid moths. We used data derived from the literature and analyzed the effects of traits both separately and simultaneously in the same model. When we analyzed the traits separately, it seemed the most important determinants of distribution change were overwintering stage and type of host plant. Nevertheless, ecological traits are often correlated and the independent effect of each trait may not be seen in analyses in which traits are analyzed separately. When we accounted for other correlated traits, the results were substantially different. Only one trait (body size), but 3 interactions, explained distribution change. This finding suggests that distribution change is not determined by 1 or 2 traits; rather, the effect of the traits depends on other interacting traits. Such complexity makes it difficult to understand the processes behind distribution changes and emphasizes the need for basic ecological knowledge of species. With such basic knowledge, a more accurate picture of the factors causing distribution changes and increasing risk of extinction might be attainable.

Population synchrony in small-world networks.

Network topography ranges from regular graphs (linkage between nearest neighbours only) via small-world graphs (some random connections between nodes) to completely random graphs. Small-world linkage is seen as a revolutionary architecture for a wide range of social, physical and biological networks, and has been shown to increase synchrony between oscillating subunits. We study small-world topographies in a novel context: dispersal linkage between spatially structured populations across a range of population models. Regular dispersal between population patches interacting with density-dependent renewal provides one ecological explanation for the large-scale synchrony seen in the temporal fluctuations of many species, for example, lynx populations in North America, voles in Fennoscandia and grouse in the UK. Introducing a small-world dispersal kernel leads to a clear reduction in synchrony with both increasing dispersal rate and small-world dispersal probability across a variety of biological scenarios. Synchrony is also reduced when populations are affected by globally correlated noise. We discuss ecological implications of small-world dispersal in the frame of spatial synchrony in population fluctuations.

Availability of prey resources drives evolution of predator-prey interaction.

Productivity is predicted to drive the ecological and evolutionary dynamics of predator-prey interaction through changes in resource allocation between different traits. Here we report results of an evolutionary experiment where prey bacteria Serratia marcescens was exposed to predatory protozoa Tetrahymena thermophila in low- and high-resource environments for approximately 2400 prey generations. Predation generally increased prey allocation to defence and caused prey selection lines to become more diverse. On average, prey became most defensive in the high-resource environment and suffered from reduced resource use ability more in the low-resource environment. As a result, the evolution of stronger prey defence in the high-resource environment led to a strong decrease in predator-to-prey ratio. Predation increased temporal variability of populations and traits of prey. However, this destabilizing effect was less pronounced in the high-resource environment. Our results demonstrate that prey resource availability can shape the trade-off allocation of prey traits, which in turn affects multiple properties of the evolving predator-prey system.

Dual-stressor selection alters eco-evolutionary dynamics in experimental communities.

Recognizing when and how rapid evolution drives ecological change is fundamental for our understanding of almost all ecological and evolutionary processes such as community assembly, genetic diversification and the stability of communities and ecosystems. Generally, rapid evolutionary change is driven through selection on genetic variation and is affected by evolutionary constraints, such as tradeoffs and pleiotropic effects, all contributing to the overall rate of evolutionary change. Each of these processes can be influenced by the presence of multiple environmental stressors reducing a population's reproductive output. Potential consequences of multistressor selection for the occurrence and strength of the link from rapid evolution to ecological change are unclear. However, understanding these is necessary for predicting when rapid evolution might drive ecological change. Here we investigate how the presence of two stressors affects this link using experimental evolution with the bacterium Pseudomonas fluorescens and its predator Tetrahymena thermophila. We show that the combination of predation and sublethal antibiotic concentrations delays the evolution of anti-predator defence and antibiotic resistance compared with the presence of only one of the two stressors. Rapid defence evolution drives stabilization of the predator-prey dynamics but this link between evolution and ecology is weaker in the two-stressor environment, where defence evolution is slower, leading to less stable population dynamics. Tracking the molecular evolution of whole populations over time shows further that mutations in different genes are favoured under multistressor selection. Overall, we show that selection by multiple stressors can significantly alter eco-evolutionary dynamics and their predictability.

Conditions for the spread of conspicuous warning signals: a numerical model with novel insights.

The initial evolution of conspicuous warning signals presents an evolutionary problem because selection against rare conspicuous signals is presumed to be strong, and new signals are rare when they first arise. Several possible solutions have been offered to solve this apparent evolutionary paradox, but disagreement persists over the plausibility of some of the proposed mechanisms. In this paper, we construct a deterministic numerical simulation model that allows us to derive the strength of selection on novel warning signals in a wide range of biologically relevant situations. We study the effects of predator psychology (learning, rate of mistaken attacks, and neophobia) on selection. We also study the how prey escape, predation intensity, number of predators, and abundance of different prey types affects selection. The model provides several important results. Selection on novel warning signals is number rather than frequency dependent. In most cases, there exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for. Signal conspicuousness (which increases detection rate) and distinctiveness (which allows predator to distinguish defended from nondefended prey) have opposing effects on evolution of warning signals. A more conspicuous warning signal cannot evolve unless it makes the prey more distinctive from palatable prey, reducing mistaken attacks by predators. A novel warning signal that is learned quickly can spread from lower abundance more easily than a signal that is learned more slowly. However, the relative rate at which the resident signal and the novel signal are learned is irrelevant for the spread of the novel signal. Long-lasting neophobia can facilitate the spread of novel warning signals. Individual selection via the ability of defended prey to escape from predator is not likely to facilitate evolution of conspicuous warning signals if both the resident (cryptic) morph and the novel morph have the same escape probability. Predation intensity (defined as the proportion of palatable prey eaten by the predator) has a strong effect on selection. More intense predation results in strong selection against rare signals, but also strong selective advantage to common signals. The threshold number of aposematic individuals is lower when predation is intense. Thus, the evolution of warning signals may be more likely in environments where predation is intense. The effect of numbers of predators depends on whether predation intensity also changes. When predation intensity is constant, increasing numbers of predators raises the threshold number of aposematic individuals, and thus makes evolution of aposematism more difficult. If predation intensity increases in parallel with number of predators, the threshold number of aposematic individuals does not change much, but selection becomes more intense on both sides of the threshold.

Negative density-distribution relationship in butterflies.

BACKGROUND: Because "laws of nature" do not exist in ecology, much of the foundations of community ecology rely on broad statistical generalisations. One of the strongest generalisations is the positive relationship between density and distribution within a given taxonomic assemblage; that is, locally abundant species are more widespread than locally sparse species. Several mechanisms have been proposed to create this positive relationship, and the testing of these mechanisms is attracting increasing attention. RESULTS: We report a strong, but counterintuitive, negative relationship between density and distribution in the butterfly fauna of Finland. With an exceptionally comprehensive data set (data includes all 95 resident species in Finland and over 1.5 million individuals), we have been able to submit several of the mechanisms to powerful direct empirical testing. Without exception, we failed to find evidence for the proposed mechanisms creating a positive density-distribution relationship. On the contrary, we found that many of the mechanisms are equally able to generate a negative relationship. CONCLUSION: We suggest that one important determinant of density-distribution relationships is the geographical location of the study: on the edge of a distribution range, suitable habitat patches are likely to be more isolated than in the core of the range. In such a situation, only the largest and best quality patches are likely to be occupied, and these by definition can support a relatively dense population leading to a negative density-distribution relationship. Finally, we conclude that generalizations about the positive density-distribution relationship should be made more cautiously.

Environmental Variation Generates Environmental Opportunist Pathogen Outbreaks.

Many socio-economically important pathogens persist and grow in the outside host environment and opportunistically invade host individuals. The environmental growth and opportunistic nature of these pathogens has received only little attention in epidemiology. Environmental reservoirs are, however, an important source of novel diseases. Thus, attempts to control these diseases require different approaches than in traditional epidemiology focusing on obligatory parasites. Conditions in the outside-host environment are prone to fluctuate over time. This variation is a potentially important driver of epidemiological dynamics and affect the evolution of novel diseases. Using a modelling approach combining the traditional SIRS models to environmental opportunist pathogens and environmental variability, we show that epidemiological dynamics of opportunist diseases are profoundly driven by the quality of environmental variability, such as the long-term predictability and magnitude of fluctuations. When comparing periodic and stochastic environmental factors, for a given variance, stochastic variation is more likely to cause outbreaks than periodic variation. This is due to the extreme values being further away from the mean. Moreover, the effects of variability depend on the underlying biology of the epidemiological system, and which part of the system is being affected. Variation in host susceptibility leads to more severe pathogen outbreaks than variation in pathogen growth rate in the environment. Positive correlation in variation on both targets can cancel the effect of variation altogether. Moreover, the severity of outbreaks is significantly reduced by increase in the duration of immunity. Uncovering these issues helps in understanding and controlling diseases caused by environmental pathogens.