Teppo Hiltunen

Predation on Multiple Trophic Levels Shapes the Evolution of Pathogen Virulence

The pathogen virulence is traditionally thought to co-evolve as a result of reciprocal selection with its host organism. In natural communities, pathogens and hosts are typically embedded within a web of interactions with other species, which could affect indirectly the pathogen virulence and host immunity through trade-offs. Here we show that selection by predation can affect both pathogen virulence and host immune defence. Exposing opportunistic bacterial pathogen Serratia marcescens to predation by protozoan Tetrahymena thermophila decreased its virulence when measured as host moth Parasemia plantaginis survival. This was probably because the bacterial anti-predatory traits were traded off with bacterial virulence factors, such as motility or resource use efficiency. However, the host survival depended also on its allocation to warning signal that is used against avian predation. When infected with most virulent ancestral bacterial strain, host larvae with a small warning signal survived better than those with an effective large signal. This suggests that larval immune defence could be traded off with effective defence against bird predators. However, the signal size had no effect on larval survival when less virulent control or evolved strains were used for infection suggesting that anti-predatory defence against avian predators, might be less constrained when the invading pathogen is rather low in virulence. Our results demonstrate that predation can be important indirect driver of the evolution of both pathogen virulence and host immunity in communities with multiple species interactions. Thus, the pathogen virulence should be viewed as a result of both past evolutionary history, and current ecological interactions.

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.

Consumer co-evolution as an important component of the eco-evolutionary feedback

Rapid evolution in ecologically relevant traits has recently been recognized to significantly alter the interaction between consumers and their resources, a key interaction in all ecological communities. While these eco-evolutionary dynamics have been shown to occur when prey populations are evolving, little is known about the role of predator evolution and co-evolution between predator and prey in this context. Here, we investigate the role of consumer co-evolution for eco-evolutionary feedback in bacteria-ciliate microcosm experiments by manipulating the initial trait variation in the predator populations. With co-evolved predators, prey evolve anti-predatory defences faster, trait values are more variable, and predator and prey population sizes are larger at the end of the experiment compared with the non-co-evolved predators. Most importantly, differences in predator traits results in a shift from evolution driving ecology, to ecology driving evolution. Thus we demonstrate that predator co-evolution has important effects on eco-evolutionary dynamics.

High Temperature and Bacteriophages Can Indirectly Select for Bacterial Pathogenicity in Environmental Reservoirs

The coincidental evolution hypothesis predicts that traits connected to bacterial pathogenicity could be indirectly selected outside the host as a correlated response to abiotic environmental conditions or different biotic species interactions. To investigate this, an opportunistic bacterial pathogen, Serratia marcescens, was cultured in the absence and presence of the lytic bacteriophage PPV (Podoviridae) at 25°C and 37°C for four weeks (Nu200a=u200a5). At the end, we measured changes in bacterial phage-resistance and potential virulence traits, and determined the pathogenicity of all bacterial selection lines in the Parasemia plantaginis insect model in vivo. Selection at 37°C increased bacterial motility and pathogenicity but only in the absence of phages. Exposure to phages increased the phage-resistance of bacteria, and this was costly in terms of decreased maximum population size in the absence of phages. However, this small-magnitude growth cost was not greater with bacteria that had evolved in high temperature regime, and no trade-off was found between phage-resistance and growth rate. As a result, phages constrained the evolution of a temperature-mediated increase in bacterial pathogenicity presumably by preferably infecting the highly motile and virulent bacteria. In more general perspective, our results suggest that the traits connected to bacterial pathogenicity could be indirectly selected as a correlated response by abiotic and biotic factors in environmental reservoirs.

Antibiotic resistance in the wild: an eco-evolutionary perspective

The legacy of the use and misuse of antibiotics in recent decades has left us with a global public health crisis: antibiotic-resistant bacteria are on the rise, making it harder to treat infections. At the same time, evolution of antibiotic resistance is probably the best-documented case of contemporary evolution. To date, research on antibiotic resistance has largely ignored the complexity of interactions that bacteria engage in. However, in natural populations, bacteria interact with other species; for example, competition and grazing are import interactions influencing bacterial population dynamics. Furthermore, antibiotic leakage to natural environments can radically alter bacterial communities. Overall, we argue that eco-evolutionary feedback loops in microbial communities can be modified by residual antibiotics and evolution of antibiotic resistance. The aim of this review is to connect some of the well-established key concepts in evolutionary biology and recent advances in the study of eco-evolutionary dynamics to research on antibiotic resistance. We also identify some key knowledge gaps related to eco-evolutionary dynamics of antibiotic resistance, and review some of the recent technical advantages in molecular microbiology that offer new opportunities for tackling these questions. Finally, we argue that using the full potential of evolutionary theory and active communication across the different fields is needed for solving this global crisis more efficiently. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences.

Temporal dynamics of a simple community with intraguild predation: an experimental test

We explore how adding complexity to a typical predator–prey interaction affects temporal dynamics. Intraguild predation webs contain competition, predation, and omnivory in a system of three species where theory and empirical results can be compared. We studied a planktonic microcosm community in which an alga is consumed by a flagellate and by a rotifer that also consumes the flagellate. Previously published theory predicts that phase lags between the species are the outcome of a “tug of war” among the intraguild-predation links: rotifers↔algae, flagellates↔algae, and rotifers↔flagellates. We observed sustained oscilltions with abundance peaks that corresponded exactly to theoretical predictions in all replicates: peaks of the rotifers and flagellates fell on either side of a quarter-period lag behind the prey (algae) peaks, with the peak of the intermediate predator (flagellates) preceding that of the top predator (rotifers). The phase lags in these experiments suggest that temporal variation in flagell...

Chapter Two - Eco-Evolutionary Dynamics in a Three-Species Food Web with Intraguild Predation: Intriguingly Complex

Abstract We explore the role of rapid evolution in the community dynamics of a three-species planktonic food web with intraguild predation. Previous studies of a two-species predator–prey system showed that rapid evolution of an anti-predator defence trait in the prey results in long-period antiphase predator–prey cycles (predator maxima coinciding with prey minima and vice versa) that are virtually diagnostic of eco-evolutionary dynamics. Here, we ask if there exist diagnostic population dynamics for a food web where algae are consumed by two predators (flagellates and rotifers), while rotifers also consume flagellates. With genetically homogeneous non-evolving prey, we previously predicted theoretically, and confirmed experimentally, that population cycles exhibit short-period oscillations with peaks in prey density followed by peaks in flagellates and then rotifers. In contrast, when prey defence can evolve, theory predicts a wide diversity of possible dynamics depending upon the trade-off between defences against the two predators. When defence against one predator implies vulnerability to the other, the predicted pattern is that predators “take turns”: one predator peaks at each prey minimum, while the other remains rare because prey are defended against it. There is strong selection for prey to evolve defence against the abundant predator (losing defence against the rare one); once this happens, predator dominance reverses rapidly. This pattern is what we generally observed in seven separate microcosms (sampled daily for 130–330 days). Cycles in which predator abundances alternate between stasis and rapid change may be explained using the concept of canards from dynamical systems theory. Nevertheless, details differed among experimental runs, making patterns diagnostic of eco-evolutionary dynamics difficult to identify.

Pulsed-resource dynamics increase the asymmetry of antagonistic coevolution between a predatory protist and a prey bacterium

Temporal resource fluctuations could affect the strength of antagonistic coevolution through population dynamics and costs of adaptation. We studied this by coevolving the prey bacterium Serratia marcescens with the predatory protozoa Tetrahymena thermophila in constant and pulsed‐resource environments for approximately 1300 prey generations. Consistent with arms race theory, the prey evolved to be more defended, whereas the predator evolved to be more efficient in consuming the bacteria. Coevolutionary adaptations were costly in terms of reduced prey growth in resource‐limited conditions and less efficient predator growth on nonliving resource medium. However, no differences in mean coevolutionary changes or adaptive costs were observed between environments, even though resource pulses increased fluctuations and mean densities of coevolving predator populations. Interestingly, a surface‐associated prey defence mechanism (bacterial biofilm), to which predators were probably unable to counter‐adapt, evolved to be stronger in pulsed‐resource environment. These results suggest that temporal resource fluctuations can increase the asymmetry of antagonistic coevolution by imposing stronger selection on one of the interacting species.

Sublethal streptomycin concentrations and lytic bacteriophage together promote resistance evolution

Sub-minimum inhibiting concentrations (sub-MICs) of antibiotics frequently occur in natural environments owing to wide-spread antibiotic leakage by human action. Even though the concentrations are very low, these sub-MICs have recently been shown to alter bacterial populations by selecting for antibiotic resistance and increasing the rate of adaptive evolution. However, studies are lacking on how these effects reverberate into key ecological interactions, such as bacteria–phage interactions. Previously, co-selection of bacteria by phages and antibiotic concentrations exceeding MICs has been hypothesized to decrease the rate of resistance evolution because of fitness costs associated with resistance mutations. By contrast, here we show that sub-MICs of the antibiotic streptomycin (Sm) increased the rate of phage resistance evolution, as well as causing extinction of the phage. Notably, Sm and the phage in combination also enhanced the evolution of Sm resistance compared with Sm alone. These observations demonstrate the potential of sub-MICs of antibiotics to impact key ecological interactions in microbial communities with evolutionary outcomes that can radically differ from those associated with high concentrations. Our findings also contribute to the understanding of ecological and evolutionary factors essential for the management of the antibiotic resistance problem. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

Protist predation can select for bacteria with lowered susceptibility to infection by lytic phages

BackgroundConsumer-resource interactions constitute one of the most common types of interspecific antagonistic interaction. In natural communities, complex species interactions are likely to affect the outcomes of reciprocal co-evolution between consumers and their resource species. Individuals face multiple enemies simultaneously, and consequently they need to adapt to several different types of enemy pressures. In this study, we assessed how protist predation affects the susceptibility of bacterial populations to infection by viral parasites, and whether there is an associated cost of defence on the competitive ability of the bacteria. As a study system we used Serratia marcescens and its lytic bacteriophage, along with two bacteriovorous protists with distinct feeding modes: Tetrahymena thermophila (particle feeder) and Acanthamoeba castellanii (surface feeder). The results were further confirmed with another study system with Pseudomonas and Tetrahymena thermophila.ResultsWe found that selection by protist predators lowered the susceptibility to infections by lytic phages in Serratia and Pseudomonas. In Serratia, concurrent selection by phages and protists led to lowered susceptibility to phage infections and this effect was independent from whether the bacteria shared a co-evolutionary history with the phage population or not. Bacteria that had evolved with phages were overall more susceptible to phage infection (compared to bacteria with history with multiple enemies) but they were less vulnerable to the phages they had co-evolved with than ancestral phages. Selection by bacterial enemies was costly in general and was seen as a lowered fitness in absence of phages, measured as a biomass yield.ConclusionsOur results show the significance of multiple species interactions on pairwise consumer-resource interaction, and suggest potential overlap in defending against predatory and parasitic enemies in microbial consumer-resource communities. Ultimately, our results could have larger scale effects on eco-evolutionary community dynamics.