Host-parasite coevolutionary arms races give way to fluctuating selection

Host-parasite coevolution is a key driver of biological diversity and parasite virulence, but its effects depend on the nature of coevolutionary dynamics over time. We used phenotypic data from coevolving populations of the bacterium Pseudomonas fluorescens SBW25 and parasitic phage SBW25Φ2, and genetic data from the phage tail fibre gene (implicated in infectivity evolution) to show that arms race dynamics, typical of short-term studies, decelerate over time. We attribute this effect to increasing costs of generalism for phages and bacteria with increasing infectivity and resistance. By contrast, fluctuating selection on individual host and parasite genotypes was maintained over time, becoming increasingly important for the phenotypic properties of parasite and host populations. Given that costs of generalism are reported for many other systems, arms races may generally give way to fluctuating selection in antagonistically coevolving populations.     

Increasing productivity accelerates host-parasite coevolution

Host-parasite coevolution is believed to influence a range of evolutionary and ecological processes, including population dynamics, evolution of diversity, sexual reproduction and parasite virulence. The impact of coevolution on these processes will depend on its rate, which is likely to be affected by the energy flowing through an ecosystem, or productivity. We addressed how productivity affected rates of coevolution during a coevolutionary arms race between experimental populations of bacteria and their parasitic viruses (phages). As hypothesized, the rate of coevolution between bacterial resistance and phage infectivity increased with increased productivity. This relationship can in part be explained by reduced competitiveness of resistant bacteria in low compared with high productivity environments, leading to weaker selection for resistance in the former. The data further suggest that variation in productivity can generate variation in selection for resistance across landscapes, a result that is crucial to the geographic mosaic theory of coevolution.     

Hot spots become cold spots: coevolution in variable temperature environments

Antagonistic coevolution between hosts and parasites is a key process in the genesis and maintenance of biological diversity. Whereas coevolutionary dynamics show distinct patterns under favourable environmental conditions, the effects of more realistic, variable conditions are largely unknown. We investigated the impact of a fluctuating environment on antagonistic coevolution in experimental microcosms of Pseudomonas fluorescens SBW25 and lytic phage SBWΦ2. High‐frequency temperature fluctuations caused no deviations from typical coevolutionary arms race dynamics. However, coevolution was stalled during periods of high temperature under intermediate‐ and low‐frequency fluctuations, generating temporary coevolutionary cold spots. Temperature variation affected population density, providing evidence that eco‐evolutionary feedbacks act through variable bacteria–phage encounter rates. Our study shows that environmental fluctuations can drive antagonistic species interactions into and out of coevolutionary cold and hot spots. Whether coevolution persists or stalls depends on the frequency of change and the environmental optima of both interacting players.     

Effects of predation on real‐time host–parasite coevolutionary dynamics

The impact of community complexity on pairwise coevolutionary dynamics is theoretically dependent on the extent to which species evolve generalised or specialised adaptations to the multiple species they interact with. Here, we show that the bacteria Pseudomonas fluorescens diversifies into defence specialists, when coevolved simultaneously with a virus and a predatory protist, as a result of fitness trade‐offs between defences against the two enemies. Strong bacteria–virus pairwise coevolution persisted, despite strong protist‐imposed selection. However, the arms race dynamic (escalation of host resistance and parasite infectivity ranges) associated with bacteria–virus coevolution broke down to a greater extent in the presence of the protist, presumably through the elevated genetic and demographic costs of increased bacteria resistance ranges. These findings suggest that strong pairwise coevolution can persist even in complex communities, when conflicting selection leads to evolutionary diversification of different defence strategies.     

Higher resources decrease fluctuating selection during host–parasite coevolution

We still know very little about how the environment influences coevolutionary dynamics. Here, we investigated both theoretically and empirically how nutrient availability affects the relative extent of escalation of resistance and infectivity (arms race dynamic; ARD) and fluctuating selection (fluctuating selection dynamic; FSD) in experimentally coevolving populations of bacteria and viruses. By comparing interactions between clones of bacteria and viruses both within‐ and between‐time points, we show that increasing nutrient availability resulted in coevolution shifting from FSD, with fluctuations in average infectivity and resistance ranges over time, to ARD. Our model shows that range fluctuations with lower nutrient availability can be explained both by elevated costs of resistance (a direct effect of nutrient availability), and reduced benefits of resistance when population sizes of hosts and parasites are lower (an indirect effect). Nutrient availability can therefore predictably and generally affect qualitative coevolutionary dynamics by both direct and indirect (mediated through ecological feedbacks) effects on costs of resistance.     

Population mixing promotes arms race host–parasite coevolution

The consequences of host–parasite coevolution are highly contingent on the qualitative coevolutionary dynamics: whether selection fluctuates (fluctuating selection dynamic; FSD), or is directional towards increasing infectivity/resistance (arms race dynamic; ARD). Both genetics and ecology can play an important role in determining whether coevolution follows FSD or ARD, but the ecological conditions under which FSD shifts to ARD, and vice versa, are not well understood. The degree of population mixing is thought to increase host exposure to parasites, hence selecting for greater resistance and infectivity ranges, and we hypothesize this promotes ARD. We tested this by coevolving bacteria and viruses in soil microcosms and found that population mixing shifted bacteria–virus coevolution from FSD to ARD. A simple theoretical model produced qualitatively similar results, showing that mechanisms that increase host exposure to parasites tend to push dynamics towards ARD. The shift from FSD to ARD with increased population mixing may help to explain variation in coevolutionary dynamics between different host–parasite systems, and more specifically the observed discrepancies between laboratory and field bacteria–virus coevolutionary studies.     

Antagonistic coevolution between a bacterium and a bacteriophage

Antagonistic coevolution between hosts and parasites is believed to play a pivotal role in host and parasite population dynamics, the evolutionary maintenance of sex and the evolution of parasite virulence. Furthermore, antagonistic coevolution is believed to be responsible for rapid differentiation of both hosts and parasites between geographically structured populations. Yet empirical evidence for host-parasite antagonistic coevolution, and its impact on between-population genetic divergence, is limited. Here we demonstrate a long-term arms race between the infectivity of a viral parasite (bacteriophage; phage) and the resistance of its bacterial host. Coevolution was largely driven by directional selection, with hosts becoming resistant to a wider range of parasite genotypes and parasites infective to a wider range of host genotypes. Coevolution followed divergent trajectories between replicate communities despite establishment with isogenic bacteria and phage, and resulted in bacteria adapted to their own, compared with other, phage populations.     

Nutrient stoichiometry shapes microbial coevolution

Coevolution is a force contributing to the generation and maintenance of biodiversity. It is influenced by environmental conditions including the scarcity of essential resources, which can drive the evolution of defence and virulence traits. We conducted a long‐term chemostat experiment where the marine cyanobacterium Synechococcus was challenged with a lytic phage under nitrogen (N) or phosphorus (P) limitation. This manipulation of nutrient stoichiometry altered the stability of host–parasite interactions and the underlying mode of coevolution. By assessing the infectivity with > 18 000 pairwise challenges, we documented directional selection for increased phage resistance, consistent with arms‐race dynamics while phage infectivity fluctuated through time, as expected when coevolution is driven by negative frequency‐dependent selection. The resulting infection networks were 50% less modular under N‐ versus P‐limitation reflecting host‐range contraction and asymmetric coevolutionary trajectories. Nutrient stoichiometry affects eco‐evolutionary feedbacks in ways that may alter the dynamics and functioning of environmental and host‐associated microbial communities.     

Eco‐evolutionary dynamics in a coevolving host–virus system

Eco‐evolutionary dynamics have been shown to be important for understanding population and community stability and their adaptive potential. However, coevolution in the framework of eco‐evolutionary theory has not been addressed directly. Combining experiments with an algal host and its viral parasite, and mathematical model analyses we show eco‐evolutionary dynamics in antagonistic coevolving populations. The interaction between antagonists initially resulted in arms race dynamics (ARD) with selective sweeps, causing oscillating host–virus population dynamics. However, ARD ended and populations stabilised after the evolution of a general resistant host, whereas a trade‐off between host resistance and growth then maintained host diversity over time (trade‐off driven dynamics). Most importantly, our study shows that the interaction between ecology and evolution had important consequences for the predictability of the mode and tempo of adaptive change and for the stability and adaptive potential of populations.     

Male-female coevolution in the wild: evidence from a time series in artemia franciscana

Sexual conflicts are ubiquitous in nature and are expected to lead to an antagonistic coevolution between the sexes. This coevolutionary process is driven by selection on sexually antagonistic traits that can either be directional or fluctuating. In this study, we used dormant cysts of Artemia franciscana, collected in the same population in three different years over a 23-year period (corresponding to ～160 generations in this system), to investigate male-female coevolution in natural conditions over time. We performed a cross experiment study where reproduction of females mated to males from the past, present, or future was monitored until death. In agreement with a model of "fluctuating selection," we found that females survived better and had longer interbrood intervals when mated with their contemporary males compared to when mated with males from the future or the past. However, female weekly and lifetime reproductive successes displayed no differences between contemporary and noncontemporary matings. Finally, the coevolutionary patterns ("arms race dynamics" or "fluctuating selection dynamics") possibly acting on female relative fitness could not be discriminated. This study is the first direct demonstration that the process of male-female coevolution, previously revealed by experimental evolution in laboratory artificial conditions, can occur in nature on a short evolutionary time scale.     

Host population bottlenecks drive parasite extinction during antagonistic coevolution

Host–parasite interactions are often characterized by large fluctuations in host population size, and we investigated how such host bottlenecks affected coevolution between a bacterium and a virus. Previous theory suggests that host bottlenecks should provide parasites with an evolutionary advantage, but instead we found that phages were rapidly driven to extinction when coevolving with hosts exposed to large genetic bottlenecks. This was caused by the stochastic loss of sensitive bacteria, which are required for phage persistence and infectivity evolution. Our findings emphasize the importance of feedbacks between ecological and coevolutionary dynamics, and how this feedback can qualitatively alter coevolutionary dynamics.     

Ongoing phenotypic and genomic changes in experimental coevolution of RNA bacteriophage Qβ and Escherichia coli

According to the Red Queen hypothesis or arms race dynamics, coevolution drives continuous adaptation and counter-adaptation. Experimental models under simplified environments consisting of bacteria and bacteriophages have been used to analyze the ongoing process of coevolution, but the analysis of both parasites and their hosts in ongoing adaptation and counter-adaptation remained to be performed at the levels of population dynamics and molecular evolution to understand how the phenotypes and genotypes of coevolving parasite-host pairs change through the arms race. Copropagation experiments with Escherichia coli and the lytic RNA bacteriophage Qβ in a spatially unstructured environment revealed coexistence for 54 days (equivalent to 163-165 replication generations of Qβ) and fitness analysis indicated that they were in an arms race. E. coli first adapted by developing partial resistance to infection and later increasing specific growth rate. The phage counter-adapted by improving release efficiency with a change in host specificity and decrease in virulence. Whole-genome analysis indicated that the phage accumulated 7.5 mutations, mainly in the A2 gene, 3.4-fold faster than in Qβ propagated alone. E. coli showed fixation of two mutations (in traQ and csdA) faster than in sole E. coli experimental evolution. These observations suggest that the virus and its host can coexist in an evolutionary arms race, despite a difference in genome mutability (i.e., mutations per genome per replication) of approximately one to three orders of magnitude.     

Differential impact of simultaneous migration on coevolving hosts and parasites

Background  

The dynamics of antagonistic host-parasite coevolution are believed to be crucially dependent on the rate of migration between populations. We addressed how the rate of simultaneous migration of host and parasite affected resistance and infectivity evolution of coevolving meta-populations of the bacterium Pseudomonas fluorescens and a viral parasite (bacteriophage). The increase in genetic variation resulting from small amounts of migration is expected to increase rates of adaptation of both host and parasite. However, previous studies suggest phages should benefit more from migration than bacteria; because in the absence of migration, phages are more genetically limited and have a lower evolutionary potential compared to the bacteria.     

Evolutionary disarmament in interspecific competition.

Competitive asymmetry, which is the advantage of having a larger body or stronger weaponry than a contestant, drives spectacular evolutionary arms races in intraspecific competition. Similar asymmetries are well documented in interspecific competition, yet they seldom lead to exaggerated traits. Here we demonstrate that two species with substantially different size may undergo parallel coevolution towards a smaller size under the same ecological conditions where a single species would exhibit an evolutionary arms race. We show that disarmament occurs for a wide range of parameters in an ecologically explicit model of competition for a single shared resource; disarmament also occurs in a simple Lotka-Volterra competition model. A key property of both models is the interplay between evolutionary dynamics and population density. The mechanism does not rely on very specific features of the model. Thus, evolutionary disarmament may be widespread and may help to explain the lack of interspecific arms races.     

Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks

The structure of mutualistic networks provides clues to processes shaping biodiversity [1-10]. Among them, interaction intimacy, the degree of biological association between partners, leads to differences in specialization patterns [4, 11] and might affect network organization [12]. Here, we investigated potential consequences of interaction intimacy for the structure and coevolution of mutualistic networks. From observed processes of selection on mutualistic interactions, it is expected that symbiotic interactions (high-interaction intimacy) will form species-poor networks characterized by compartmentalization [12, 13], whereas nonsymbiotic interactions (low intimacy) will lead to species-rich, nested networks in which there is a core of generalists and specialists often interact with generalists [3, 5, 7, 12, 14]. We demonstrated an association between interaction intimacy and structure in 19 ant-plant mutualistic networks. Through numerical simulations, we found that network structure of different forms of mutualism affects evolutionary change in distinct ways. Change in one species affects primarily one mutualistic partner in symbiotic interactions but might affect multiple partners in nonsymbiotic interactions. We hypothesize that coevolution in symbiotic interactions is characterized by frequent reciprocal changes between few partners, but coevolution in nonsymbiotic networks might show rare bursts of changes in which many species respond to evolutionary changes in a single species.     

The Impact of Resource Availability on Bacterial Resistance to Phages in Soil

Resource availability can affect the coevolutionary dynamics between host and parasites, shaping communities and hence ecosystem function. A key finding from theoretical and in vitro studies is that host resistance evolves to greater levels with increased resources, but the relevance to natural communities is less clear. We took two complementary approaches to investigate the effect of resource availability on the evolution of bacterial resistance to phages in soil. First, we measured the resistance and infectivity of natural communities of soil bacteria and phage in the presence and absence of nutrient-providing plants. Second, we followed the real-time coevolution between defined bacteria and phage populations with resource availability manipulated by the addition or not of an artificial plant root exudate. Increased resource availability resulted in increases in bacterial resistance to phages, but without a concomitant increase in phage infectivity. These results suggest that phages may have a reduced impact on the control of bacterial densities and community composition in stable, high resource environments.     

Two modes of host–enemy coevolution

The process of coevolution between host and enemy has traditionally been viewed as an evolutionary arms race between resistance and counterresistance. The arms-race metaphor of coevolution is widely accepted because it explains the evolution of many characters in species involved in host–enemy interactions. However, molecular work in plant–pathogen systems suggests a coevolutionary interplay between plant recognition of an attacking pathogen and pathogen evasion from recognition. We refer to this process as information coevolution, and contrast this with arms race coevolution to show that these two processes result in very different patterns of host resistance and enemy virulence at the population level. First, information coevolution results in a lower proportion of hosts that are susceptible to enemy attack within a population. Second, information coevolution produces a pattern of local maladaptation of enemy on host, a naturally occurring phenomenon that is difficult to explain under arms race coevolution. We then conduct a literature review to survey the empirical support for either mode of coevolution using the predicted patterns of host resistance and enemy virulence. Evidence supports both modes of coevolution in plant–enemy interactions, whereas no support is found for information coevolution in vertebrate–parasite and invertebrate–parasite systems.     

Inferring coevolution in a plant–pollinator network

Mutualistic interactions are at the core of community dynamics, determining dispersal, colonization and differential survival and reproduction among individuals and species. Mutualistic interactions therefore affect the fitness of interaction partners, hence modifying their respective evolutionary trajectories reciprocally, potentially leading to coevolution. Although mathematical models predict coevolution in mutualistic interaction networks, no empirical data are available. By taking into account the patterns of interactions and reconstructing evolutionary change in plant and pollinator traits, we tested the hypothesis that coevolution occurs between plants and insects that interact more frequently, or more symmetrically. To test this hypothesis, we built an interaction network with data from five flowering seasons, measured plant and insect morphology, mapped morphology on the plant and insect phylogenies, and reconstructed ancestral character changes based on maximum parsimony. We calculated an index, called the coevolutionary ratio, which represents the amount of correlated change in traits that mediate the interaction between plants and pollinators (i.e. proboscis versus corolla length, and body width and corolla aperture). Our results suggest that high frequency of interaction, i.e. the number of times two species interact, does not lead to coevolution. Instead, symmetry of interaction strength, i.e. the reciprocal similarity in the mutual effect of interaction partners, may lead to coevolution, in spite of a pervasive lack of reciprocal specialization and high interaction frequency. Although the statistical signal is quite weak, our results hold for three statistical tests of very different nature. The most specialized species, expected to be under directional selection, do not show more evolutionary change than do generalist species, expected to be under different, perhaps opposing, selective pressures. By dissecting the complexity of an interaction network we show that coevolution may partially shape functional morphology of interaction partners, thus providing the closest evidence to date of mutualistic adaptation of organisms within a community.     

Relationships between ecological interaction modifications and diffuse coevolution: similarities, differences, and causal links

A major empirical approach in community ecology is to describe the dynamics of a community by examining small subsets of species. Unfortunately, interaction modifications, which cause pair-wise interaction coefficients to depend on the presence or absence of additional species, can make it difficult to predict the overall dynamics of species within a community from experiments with pairs of species. In a similar fashion, one of the major approaches in evolutionary ecology has been to describe the likely evolutionary dynamics of a single species by focusing on the selection imposed by a limited number of other species within the community. However, recent work on diffuse coevolution indicates that selection pressures due to one species can change in the presence of other species. The magnitude of the difficulty that interaction modifications and diffuse coevolution present for predicting ecological and evolutionary dynamics is an unresolved question. Here we outline the similarities and differences between the two topics, discuss experimental and statistical approaches to studying them, and make predictions about when ecological interaction modifications are likely to cause diffuse coevolution. Since the currencies for interaction modifications are usually fitness components such as growth, fecundity, or survival, is it likely that these will translate into corresponding differences in the relative fitness of individuals or genotypes, and thus in general these two phenomena will occur together. We argue that community ecologists and evolutionary ecologists will both benefit from experiments that test for the effects of interaction modifications, and that studies of the mechanisms driving interaction modifications and diffuse coevolution (e.g., changes in behavior, nonlinear effects on shared resources, genetic covariances) will aid our progress in understanding the ecological and evolutionary dynamics of communities.     

Coevolution can stabilize a mutualistic interaction

Interspecific mutualisms are ubiquitous in nature, despite their ecological and evolutionary instability. Recent studies have developed coevolutionary theory of mutualisms, which coupled population and evolutionary dynamics, to resolve the longstanding puzzle. However, earlier studies assumed a time-scale separation between these dynamics, leaving an unanswered question of how a relaxation in the time-scale separation affects the coevolutionary dynamics of mutualism. Here I relax the strong assumption to theoretically show that ecological and evolutionary dynamics occurring in a similar time scale can stabilize an otherwise unstable mutualism. I show that the coevolutionary dynamics can cause a stable limit cycle or stable equilibrium in the population sizes, even if the population sizes increase unbounded in the absence of evolutionary adaptation. In contrast, coevolution can also cause stable limit cycle even if the population dynamics is stable in the absence of evolutionary adaptation. Furthermore, the model predicts that the population dynamics is likely to converge to equilibrium when the evolutionary speed of two species is similar and fast or highly dissimilar. The results suggest that the ease of the evolutionary ‘arms race’ is of crucial importance to maintain mutualism.