6789804
Rapidly fluctuating environments constrain coevolutionary arms races by impeding selective sweeps
Although pervasive, the impact of temporal environmental heterogeneity on coevolutionary processes is poorly understood. Productivity is a key temporally heterogeneous variable, and increasing productivity has been shown to increase rates of antagonistic arms race coevolution, and lead to the evolution of more broadly resistant hosts and more broadly infectious parasites. We investigated the effects of the grain of environmental heterogeneity, in terms of fluctuations in productivity, on bacteria–phage coevolution. Our findings demonstrate that environmental heterogeneity could constrain antagonistic coevolution, but that its effect was dependent upon the grain of heterogeneity, such that both the rate and extent of coevolution were most strongly limited in fine-grained, rapidly fluctuating heterogeneous environments. We further demonstrate that rapid environmental fluctuations were likely to have impeded selective sweeps of resistance alleles, which occurred over longer durations than the fastest, but not the slowest, frequency of fluctuations used. Taken together our results suggest that fine-grained environmental heterogeneity constrained the coevolutionary arms race by impeding selective sweeps.
41557923
Environment can alter selection in host-parasite interactions.
Characteristics of hosts and parasites have a genetic basis, and thus can be shaped by coevolution. Infections measured under laboratory conditions have shown that the environment in which hosts and parasites interact might substantially affect the strength and specificity of selection. In addition, various components of host-parasite fitness are differentially altered by the environment. Despite this, environmental fluctuations are often excluded from experimental coevolutionary studies and theoretical models as 'noise'. Because most host-parasite interactions exist in heterogeneous environments, we argue that there is a need to incorporate fluctuating environments into future empirical and theoretical work on host-parasite coevolution.
83132850
The Geographic Mosaic of Coevolution
Coevolution - reciprocal evolutionary change in interacting species driven by natural selection - is one of the most important ecological and genetic processes organizing the earth's biodiversity: most plants and animals require coevolved interactions with other species to survive and reproduce. The Geographic Mosaic of Coevolution analyzes how the biology of species provides the raw material for long-term coevolution, evaluates how local coadaptation forms the basic module of coevolutionary change, and explores how the coevolutionary process reshapes locally coevolving interactions across the earth's constantly changing landscapes. Picking up where his influential The Coevolutionary Process left off, John N. Thompson synthesizes the state of a rapidly developing science that integrates approaches from evolutionary ecology, population genetics, phylogeography, systematics, evolutionary biochemistry and physiology, and molecular biology. Using models, data, and hypotheses to develop a complete conceptual framework, Thompson also draws on examples from a wide range of taxa and environments, illustrating the expanding breadth and depth of research in coevolutionary biology.
1095270
Role of coevolution in generating biological diversity: spatially divergent selection trajectories.
The Geographic Mosaic Theory of Coevolution predicts that divergent coevolutionary selection produces genetic differentiation across populations. The 29 studies reviewed here support this hypothesis as they all report spatially diverged selection trajectories which have generated variable outcomes in the interaction traits among populations. This holds for both mutualistic interactions such as those between host plants and their root symbionts, or plants and their pollinators, as well as for antagonistic interactions such as plants and their pathogens or herbivores. Most often, it is the strength of selection that varies across landscapes. Variation may be generated by both the physical environment (namely temperature), and the local community--competitors, parasites, and alternative hosts--that intensify or dilute selection locally for a wide range of species interactions. At its extreme, selection trajectories may be reversed with an antagonistic interaction being commensalistic in some populations and mutualistic in yet others, depending on the local community context. Selection trajectories were found to diverge among continents, but also more locally among neighbouring populations and even within a single population. This result highlights the importance of coevolutionary selection generating biological diversity with far-reaching implications for both biodiversity conservation as well as applied biology.
46149297
Temperature-dependent transmission and latency of Holospora undulata, a micronucleus-specific parasite of the ciliate Paramecium caudatum
Transmission of parasites to new hosts crucially depends on the timing of production of transmission stages and their capacity to start an infection. These parameters may be influenced by genetic factors, but also by the environment. We tested the effects of temperature and host genotype on infection probability and latency in experimental populations of the ciliate Paramecium caudatum, after exposure to infectious forms of its bacterial parasite Holospora undulata. Temperature had a significant effect on the expression of genetic variation for transmission and maintenance of infection. Overall, low temperature (10 °C) increased levels of (multiple) infection, but arrested parasite development; higher temperatures (23 and 30 °C) accelerated the onset of production of infectious forms, but limited transmission success. Viability of infectious forms declined rapidly at 23 and 30 °C, thereby narrowing the time window for transmission. Thus, environmental conditions can generate trade-offs between transmission relevant parameters and alter levels of multiple infection or parasite-mediated selection, which may affect evolutionary trajectories of parasite life history or virulence.
16612831
Pathogen fitness components and genotypes differ in their sensitivity to nutrient and temperature variation in a wild plant–pathogen association
Understanding processes maintaining variation in pathogen life‐history stages affecting infectivity and reproduction is a key challenge in evolutionary ecology. Models of host–parasite coevolution are based on the assumption that genetic variation for host–parasite interactions is a significant cause of variation in infection, and that variation in environmental conditions does not overwhelm the genetic basis. However, surprisingly little is known about the stability of genotype–genotype interactions under variable environmental conditions. Here, using a naturally occurring plant–pathogen interaction, I tested whether the two distinct aspects of the infection process – infectivity and transmission potential – vary over realistic nutrient and temperature gradients. I show that the initial pathogen infectivity and host resistance responses are robust over the environmental gradients. However, for compatible responses there were striking differences in how different pathogen life‐history stages and host and pathogen genotypes responded to environmental variation. For some pathogen genotypes even slight changes in temperature arrested spore production, rendering the developing infection ineffectual. The response of pathogen genotypes to environmental gradients varied in magnitude and even direction, so that their rankings changed across the abiotic gradients. Hence, the variable environment of spatially structured host–parasite interactions may strongly influence the maintenance of polymorphism in pathogen life‐history stages governing transmission, whereas evolutionary trajectories of infectivity may be unaffected by the surrounding environment.
15099429
Environmental influence on the genetic basis of mosquito resistance to malaria parasites
The genetic basis of a host's resistance to parasites has important epidemiological and evolutionary consequences. Understanding this genetic basis can be complicated by non-genetic factors, such as environmental quality, which may influence the expression of genetic resistance and profoundly alter patterns of disease and the host's response to selection. In particular, understanding the environmental influence on the genetic resistance of mosquitoes to malaria gives valuable knowledge concerning the use of malaria-resistant transgenic mosquitoes as a measure of malaria control. We made a step towards this understanding by challenging eight isofemale lines of the malaria vector Anopheles stephensi with the rodent malaria parasite Plasmodium yoelii yoelii and by feeding the mosquitoes with different concentrations of glucose. The isofemale lines differed in infection loads (the numbers of oocysts), corroborating earlier studies showing a genetic basis of resistance. In contrast, the proportion of infected mosquitoes did not differ among lines, suggesting that the genetic component underlying infection load differs from the genetic component underlying infection rate. In addition, the mean infection load and, in particular, its heritable variation in mosquitoes depended on the concentration of glucose, which suggests that the environment affects the expression and the evolution of the mosquitoes' resistance in nature. We found no evidence of genotype-by-environment interactions, i.e. the lines responded similarly to environmental variation. Overall, these results indicate that environmental variation can significantly reduce the importance of genes in determining the resistance of mosquitoes to malaria infection.
198158239
HOST-PARASITE AND GENOTYPE-BY-ENVIRONMENT INTERACTIONS: TEMPERATURE MODIFIES POTENTIAL FOR SELECTION BY A STERILIZING PATHOGEN
Abstract Parasite-mediated selection is potentially of great importance in modulating genetic diversity. Genetic variation for resistance, the fuel for natural selection, appears to be common in host-parasite interactions, but responses to selection are rarely observed. In the present study, we tested whether environmental variation could mediate infection and determine evolutionary outcomes. Temperature was shown to dramatically alter the potential for parasite-mediated selection in two independent laboratory infection experiments at four temperatures. The bacterial parasite, Pasteuria ramosa, was extremely virulent at 20°C and 25°C, sterilizing its host, Daphnia magna, so that females often never produced a single brood. However, at 10°C and 15°C, the host-parasite interaction was much more benign, as nearly all females produced broods before becoming sterile. This association between virulence and temperature alone could stabilize coexistence and lead to the maintenance of diversity, because it would weaken parasite-mediated selection during parts of the season. Additionally, highly significant genotype-by-environment interactions were found, with changes in clone rank order for infection rates at different temperatures. Our results clearly show that the outcome of parasite-mediated selection in this system is strongly context dependent.
11237373
Temperature‐dependent costs of parasitism and maintenance of polymorphism under genotype‐by‐environment interactions
The maintenance of genetic variation for infection‐related traits is often attributed to coevolution between hosts and parasites, but it can also be maintained by environmental variation if the relative fitness of different genotypes changes with environmental variation. To gain insight into how infection‐related traits are sensitive to environmental variation, we exposed a single host genotype of the freshwater crustacean Daphnia magna to four parasite isolates (which we assume to represent different genotypes) of its naturally co‐occurring parasite Pasteuria ramosa at 15, 20 and 25 °C. We found that the cost to the host of becoming infected varied with temperature, but the magnitude of this cost did not depend on the parasite isolate. Temperature influenced parasite fitness traits; we found parasite genotype‐by‐environment (G × E) interactions for parasite transmission stage production, suggesting the potential for temperature variation to maintain genetic variation in this trait. Finally, we tested for temperature‐dependent relationships between host and parasite fitness traits that form a key component of models of virulence evolution, and we found them to be stable across temperatures.
86603336
Ecology: From Individuals to Ecosystems
Preface.Introduction.Part 1. ORGANISMS .1. Organisms in their environments: the evolutionary backdrop.2. Conditions.3. Resources.4. Life, death and life histories.5. Intraspecific competition.6. Dispersal, dormancy and metapopulations.7. Ecological applications at the level of organisms and single-species populations Part 2. SPECIES INTERACTIONS.8. Interspecific competition.9. The nature of predation.10. The population dynamics of predation.11. Decomposers and detritivores.12. Parasitism and disease.13. Symbiosis and mutualism.14. Abundance.15. Ecological applications at the level of population interactions Part 3. COMMUNITIES AND ECOSYSTEMS .16. The nature of the community.17. The flux of energy through ecosystems.18. The flux of matter through ecosystems.19. The influence of population interactions on community structure.20. Food webs.21. Patterns in species richness.22. Ecological applications at the level of communities and ecosystems.References.Organism Index.Subject Index
4422424
Antagonistic Coevolution over Productivity Gradients
This study addresses the question of how spatial heterogeneity in prey productivity and migration act to determine geographic patterns in antagonistic coevolution with a predator. We develop and analyze a quantitative coevolutionary model for a predator‐prey interaction. If the model is modified appropriately, the results could broadly apply to multispecies communities and to herbivore‐plant, parasite‐host, and parasitoid‐host associations. Model populations are distributed over a gradient in prey birth rate (as a measure of productivity). Each population, in each patch, is made up of a suite of strains. Each strain of the predator has a certain ability to successfully attack each strain of the prey. We consider scenarios of isolated patches, global migration, and stepping‐stone (i.e., local) migration over a linear string of patches. The most pervasive patterns are the following: investments in predator offense and prey defense are both maximal in the patches of highest prey productivity; when there are no constraints on maximal investment, mean predation evolves to highest levels in the most productive patches; similarly, the predator has a greater impact (measured as the percentage reduction in prey density) on the prey population in high productivity patches as compared with low productivity ones—in spite (even after evolution) of prey abundance being highest in the most productive patches; and migration has the net effect of shunting relatively offensive and defensive strains from productive patches to nonproductive ones, potentially resulting in the elimination of otherwise rare, low‐investment clones. A modification of the model to gene‐for‐gene type interactions predicts that generalist strains (in terms of the range of strains the predator can exploit or the prey can fend off) dominate in productive areas of the prey, whereas specialists prevail in marginal habitats. Assuming a wide range of productivities over the prey's geographical distribution, the greatest strain diversity should be found in habitats of intermediate productivity. We discuss the implications of our study for adaptation and conservation. Empirical studies are in broad accord with our findings.
40568370
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.
531593
Trophic network structure emerges through antagonistic coevolution in temporally varying environments
Understanding the mechanisms underlying ecological specialization is central to our understanding of community ecology and evolution. Although theoretical work has investigated how variable environments may affect specialization in single species, little is known about how such variation impacts bipartite network structure in antagonistically coevolving systems. Here, we develop and analyse a general model of victim–enemy coevolution that explicitly includes resource and population dynamics. We investigate how temporal environmental heterogeneity affects the evolution of specialization and associated community structure. Environmental productivity influences victim investment in resistance, which will shape patterns of specialization through its regulating effect on enemy investment in infectivity. We also investigate the epidemiological consequences of environmental variability and show that enemy population density is maximized for intermediate lengths of productive seasons, which corresponds to situations where enemies can evolve higher infectivity than victims can evolve defence. We discuss our results in the light of empirical studies, and further highlight ways in which our model applies to a range of natural systems.
86301123
Population mixing accelerates coevolution
Theory predicts that mixing in spatially structured populations of hosts and parasites can increase the rate of antagonistic coevolution. We experimentally tested this prediction by allowing populations of bacteria (Pseudomonas fluorescens) and parasitic bacteriophage to coevolve in mixed and unmixed microcosms. Coevolution proceeded at approximately twice the rate in mixed populations compared with unmixed populations and caused the evolution of more resistant hosts and more infective parasites.
46246120
Abiotic heterogeneity drives parasite local adaptation in coevolving bacteria and phages
Spatial abiotic heterogeneity can result in divergent selection, hence might increase the magnitude of host–parasite local adaptation (the mean difference in fitness of sympatric vs. allopatric host–parasite combinations). We explicitly tested this hypothesis by measuring local adaptation in experimentally coevolved populations of bacteria and viruses evolved in the same or different nutrient media. Consistent with previous work, we found that mean levels of evolved phage infectivity and bacteria resistance varied with nutrient concentration, with maximal levels at nutrient concentrations that supported the greatest densities of bacteria. Despite this variation in evolved mean infectivity and resistance between treatments, we found that parasite local adaptation was greatly increased when measured between populations evolved in different, compared with the same, media. This pattern is likely to have resulted from different media imposing divergent selection on bacterial hosts, and phages in turn adapting to their local hosts. These results demonstrate that the abiotic environment can play a strong and predictable role in driving patterns of local adaptation.
16460466
Coevolution in Temporally Variable Environments
Many potentially mutualistic interactions are conditional, with selection that varies between mutualism and antagonism over space and time. We develop a genetic model of temporally variable coevolution that incorporates stochastic fluctuations between mutualism and antagonism. We use this model to determine conditions necessary for the coevolution of matching traits between a host and a conditional mutualist. Using an analytical approximation, we show that matching traits will coevolve when the geometric mean interaction is mutualistic. When this condition does not hold, polymorphism and trait mismatching are maintained, and coevolutionary cycles may result. Numerical simulations verify this prediction and suggest that it remains robust in the presence of temporal autocorrelation. These results are compared with those from spatial models with unrestricted movement. The comparisons demonstrate that gene flow is unnecessary for generating empirical patterns predicted by the geographic mosaic theory of coevolution.
23702293
Antagonistic coevolution across productivity gradients: an experimental test of the effects of dispersal
Coevolution commonly occurs in spatially heterogeneous environments, resulting in variable selection pressures acting on coevolving species. Dispersal across such environments is predicted to have a major impact on local coevolutionary dynamics. Here, we address how co‐dispersal of coevolving populations of host and parasite across an environmental productivity gradient affected coevolution in experimental populations of bacteria and their parasitic viruses (phages). The rate of coevolution between bacteria and phages was greater in high‐productivity environments. High‐productivity immigrants (∼2% of the recipient population) caused coevolutionary dynamics (rates of coevolution and degree of generalist evolution) in low‐productivity environments to be largely indistinguishable from high‐productivity environments, whereas immigration from low‐productivity environments (∼0.5% of the population) had no discernable impact. These results could not be explained by demography alone, but rather high‐productivity immigrants had a selective advantage in low‐productivity environments, but not vice versa. Coevolutionary interactions in high‐productivity environments are therefore likely to have a disproportionate impact on coevolution across the landscape as a whole.
2519801
Gene Flow Reverses an Adaptive Cline in a Coevolving Host‐Parasitoid Interaction
Many natural populations are characterized by clinal patterns of adaptation, but it is unclear how gene flow and environmental gradients interact to drive such clines. We addressed this question by directly manipulating dispersal and productivity in an experimental landscape containing a microbial parasitoid, the bacteriophage T7, and its host, the bacterium Escherichia coli. We observed that the adaptation of parasitoids increased on hosts originating from lower‐productivity communities in the absence of gene flow. However, adaptation decreased along the same productivity gradient with experimentally imposed gene flow of the host and parasitoid. This occurred despite relatively low rates of gene flow.
4082648
Adaptation varies through space and time in a coevolving host–parasitoid interaction
One of the central challenges of evolutionary biology is to understand how coevolution organizes biodiversity over complex geographic landscapes. Most species are collections of genetically differentiated populations, and these populations have the potential to become adapted to their local environments in different ways. The geographic mosaic theory of coevolution incorporates this idea by proposing that spatial variation in natural selection and gene flow across a landscape can shape local coevolutionary dynamics. These effects may be particularly strong when populations differ across productivity gradients, where gene flow will often be asymmetric among populations. Conclusive empirical tests of this theory have been particularly difficult to perform because they require knowledge of patterns of gene flow, historical population relationships and local selection pressures. We have tested these predictions empirically using a model community of bacteria and bacteriophage (viral parasitoids of bacteria). We show that gene flow across a spatially structured landscape alters coevolution of parasitoids and their hosts and that the resulting patterns of adaptation can fluctuate in both space and time.
9285803
Source Populations Act as Coevolutionary Pacemakers in Experimental Selection Mosaics Containing Hotspots and Coldspots
Natural populations of hosts and their enemies are often spatially structured, with patches that vary in the strength of reciprocal selection, so‐called coevolutionary hotspots and coldspots with strong or weak reciprocal selection, respectively. Theory predicts that dispersal from hotspots should intensify coevolution in coldspots, whereas dispersal from coldspots should weaken coevolution in hotspots; however, there have been few empirical tests. We addressed this using paired populations of the bacterium Pseudomonas fluorescens and the phage SBW25Φ2 linked by one‐way dispersal. Within each population, the strength of reciprocal selection was manipulated by altering the bacteria‐phage encounter rate, which changes the rate of coevolution without affecting environmental productivity. We observed that dispersal from hotspots accelerated coevolution in coldspots, while dispersal from coldspots decelerated coevolution in hotspots. These results confirm theoretical predictions and suggest that source populations can act as coevolutionary “pacemakers” for recipient populations, overriding local conditions.
4442185
Hot Spots, Cold Spots, and the Geographic Mosaic Theory of Coevolution
Species interactions commonly coevolve as complex geographic mosaics of populations shaped by differences in local selection and gene flow. We use a haploid matching‐alleles model for coevolution to evaluate how a pair of species coevolves when fitness interactions are reciprocal in some locations (“hot spots”) but not in others (“cold spots”). Our analyses consider mutualistic and antagonistic interspecific interactions and a variety of gene flow patterns between hot and cold spots. We found that hot and cold spots together with gene flow influence coevolutionary dynamics in four important ways. First, hot spots need not be ubiquitous to have a global influence on evolution, although rare hot spots will not have a disproportionate impact unless selection is relatively strong there. Second, asymmetries in gene flow can influence local adaptation, sometimes creating stable equilibria at which species experience minimal fitness in hot spots and maximal fitness in cold spots, or vice versa. Third, asymmetries in gene flow are no more important than asymmetries in population regulation for determining the maintenance of local polymorphisms through coevolution. Fourth, intraspecific allele frequency differences among hot and cold spot populations evolve under some, but not all, conditions. That is, selection mosaics are indeed capable of producing spatially variable coevolutionary outcomes across the landscapes over which species interact. Altogether, our analyses indicate that coevolutionary trajectories can be strongly shaped by the geographic distribution of coevolutionary hot and cold spots, and by the pattern of gene flow among populations.
86354825
GENETIC POLYMORPHISM IN HETEROGENEOUS ENVIRONMENTS: A DECADE LATER
Ten years ago, Joseph Felsenstein (35) and I (56) both wrote reviews discussing the maintenance of genetic polymorphisms in heterogeneous environments. I addressed the question of the importance in maintaining genetic variation of diversifying selection (sometimes called the niche-variation hypothesis), i.e. selection for different alleles in different environments. My focus was on the evidence and theory supporting the connection of a variable environment with genetic variation, particularly as an explanation for the large amounts of allozymic variation. At that time, the empirical evidence suggesting a genetic-environment connection for allozymic variation was mostly correlative and not in general experimentally based. Theory suggested, however, that polymorphism maintenance was possible in a variable environment; it was most likely when there was variable selection in space and limited gene flow and/or habitat selection. The purpose of this review is to evaluate the research of the intervening decade on genetic polymorphism in variable environments. The topics of this review are divided in a fashion similar to that of the earlier review. First, I mention some recent work in which there has been detailed investigation of the relationship of different environments and the maintenance of genetic variation. Second, I review the theoretical developments in the past decade. Finally, I discuss recent experimental work in some detail. An emphasis in the review is to evaluate these experimental studies, a number of which were designed specifically to determine the importance of heterogeneous environments in maintaining genetic variation.
31830188
Pulsed-Resource Dynamics Constrain the Evolution of Predator-Prey Interactions
Although temporal variability in the physical environment plays a major role in population fluctuations, little is known about how it drives the ecological and evolutionary dynamics of species interactions. We studied experimentally how extrinsic resource pulses affect evolutionary and ecological dynamics between the prey bacterium Serratia marcescens and the predatory protozoan Tetrahymena thermophila. Predation increased the frequency of defensive, nonpigmented prey types, which bore competitive costs in terms of reduced maximum growth rate, most in a constant-resource environment. Furthermore, the predator densities of the pulsed-resource environment regularly fluctuated above and below the mean predator densities of the constant environment. These results suggest that selection favored fast-growing competitor prey types over defensive but slower-growing prey types more often in the pulsed-resource environment (abundance of resources and low predation risk). As a result, the selection for prey defense fluctuated more in the pulsed-resource environment, leading to a weaker mean response in prey defense. At the ecological level, the evolution of prey defense weakened the relative strength of top-down regulation on prey community. This was more evident in the constant-resource environment, whereas the slow emergence of defensive prey types gradually decreased the amplitude of predator peaks in the pulsed-resource environment. Our study suggests that rapid evolution plays a smaller role in the ecological dynamics of communities dominated by resource pulses.
25103925
The impact of environmental change on host–parasite coevolutionary dynamics
Environmental factors are known to affect the strength and the specificity of interactions between hosts and parasites. However, how this shapes patterns of coevolutionary dynamics is not clear. Here, we construct a simple mathematical model to study the effect of environmental change on host–parasite coevolutionary outcome when interactions are of the matching-alleles or the gene-for-gene type. Environmental changes may effectively alter the selective pressure and the level of specialism in the population. Our results suggest that environmental change altering the specificity of selection in antagonistic interactions can produce alternating time windows of cyclical allele-frequency dynamics and cessation thereof. This type of environmental impact can also explain the maintenance of polymorphism in gene-for-gene interactions without costs. Overall, our study points to the potential consequences of environmental variation in coevolution, and thus the importance of characterizing genotype-by-genotype-by-environment interactions in natural host–parasite systems, especially those that change the direction of selection acting between the two species.
25236703
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.
33351508
Experimental coevolution of species interactions.
Coevolution, the process of reciprocal adaptation and counter-adaptation between ecologically interacting species, affects most organisms and is considered a key force structuring biological diversity. Our understanding of the pattern and process of coevolution, particularly of antagonistic species interactions, has been hugely advanced in recent years by an upsurge in experimental studies that directly observe coevolution in the laboratory. These experiments pose new questions by revealing novel facets of the coevolutionary process not captured by current theory, while also providing the first empirical tests of longstanding coevolutionary ideas, including the influential Red Queen hypothesis. In this article, we highlight emerging directions for this field, including experimental coevolution of mutualistic interactions and understanding how pairwise coevolutionary processes scale up within species-rich communities.
9742305
Experimental coevolution with bacteria and phage. The Pseudomonas fluorescens--Phi2 model system.
Parasites are ubiquitous in biological systems and antagonistic coevolution between hosts and parasites is thought be a major ecological and evolutionary force. Recent experiments using laboratory populations of bacteria and their parasitic viruses, phage, have provided the first direct empirical evidence of antagonistic coevolution in action. In this article we describe this model system and synthesise recent findings that address the causes and consequences of antagonistic coevolution.
3527152
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.
28715888
The impact of parasite dispersal on antagonistic host–parasite coevolution
Coevolving populations of hosts and parasites are often subdivided into a set of patches connected by dispersal. Higher relative rates of parasite compared with host dispersal are expected to lead to parasite local adaptation. However, we know of no studies that have considered the implications of higher relative rates of parasite dispersal for other aspects of the coevolutionary process, such as the rate of coevolution and extent of evolutionary escalation of resistance and infectivity traits. We investigated the effect of phage dispersal on coevolution in experimental metapopulations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage SBW25Φ2. Both the rate of coevolution and the breadth of evolved infectivity and resistance ranges peaked at intermediate rates of parasite dispersal. These results suggest that parasite dispersal can enhance the evolutionary potential of parasites through provision of novel genetic variation, but that high rates of parasite dispersal can impede the evolution of parasites by homogenizing genetic variation between patches, thereby constraining coevolution.
1356167
Differential impact of simultaneous migration on coevolving hosts and parasites
BackgroundThe 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.ResultsThe results supported the hypothesis: migration increased the resistance of bacteria to their local (sympatric) hosts. Moreover, migration benefited phages more than hosts with respect to 'global' (measured with respect to the whole range of migration regimes) patterns of resistance and infectivity, because of the differential evolutionary responses of bacteria and phage to different migration regimes. Specifically, we found bacterial global resistance peaked at intermediate rates of migration, whereas phage global infectivity plateaued when migration rates were greater than zero.ConclusionThese results suggest that simultaneous migration of hosts and parasites can dramatically affect the interaction of host and parasite. More specifically, the organism with the lower evolutionary potential may gain the greater evolutionary advantage from migration.
21384374
Construction and validation of a neutrally-marked strain of Pseudomonas fluorescens SBW25.
Neutrally marked bacterial strains are useful in many experimental evolution and molecular ecology studies to assess the relative fitness of a given strain. Here we describe the construction and validation of a neutral marker for the model organism Pseudomonas fluorescens SBW25. The marked strain, called SBW25-lacZ, was created by integrating a promoterless 'lacZ into the defective prophage locus of the SBW25 chromosome. Fitness assays conducted in various laboratory media and in planta revealed that the fitness levels of SBW25-lacZ were comparable with the wild-type ancestor.
4364925
Antagonistic coevolution accelerates molecular evolution
The Red Queen hypothesis proposes that coevolution of interacting species (such as hosts and parasites) should drive molecular evolution through continual natural selection for adaptation and counter-adaptation. Although the divergence observed at some host-resistance and parasite-infectivity genes is consistent with this, the long time periods typically required to study coevolution have so far prevented any direct empirical test. Here we show, using experimental populations of the bacterium Pseudomonas fluorescens SBW25 and its viral parasite, phage Φ2 (refs 10, 11), that the rate of molecular evolution in the phage was far higher when both bacterium and phage coevolved with each other than when phage evolved against a constant host genotype. Coevolution also resulted in far greater genetic divergence between replicate populations, which was correlated with the range of hosts that coevolved phage were able to infect. Consistent with this, the most rapidly evolving phage genes under coevolution were those involved in host infection. These results demonstrate, at both the genomic and phenotypic level, that antagonistic coevolution is a cause of rapid and divergent evolution, and is likely to be a major driver of evolutionary change within species.
25818075
Genetic basis of infectivity evolution in a bacteriophage
Antagonistic coevolution between hosts and parasites is probably ubiquitous. However, very little is known of the genetic changes associated with parasite infectivity evolution during adaptation to a coevolving host. We followed the phenotypic and genetic changes in a lytic virus population (bacteriophage; phage Φ2) that coevolved with its bacterial host, Pseudomonas fluorescens SBW25. First, we show the rapid evolution of numerous unique phage infectivity phenotypes, and that both phage host range and bacterial resistance to individual phage increased over coevolutionary time. Second, each of the distinct phage phenotypes in our study had a unique genotype, and molecular evolution did not act uniformly across the phage genome during coevolution. In particular, we detected numerous substitutions on the tail fibre gene, which is involved in the first step of the host–parasite interaction: host adsorption. None of the observed mutations could be directly linked with infection against a particular host, suggesting that the phenotypic effects of infectivity mutations are probably epistatic. However, phage genotypes with the broadest host ranges had the largest number of nonsynonymous amino acid changes on genes implicated in infectivity evolution. An understanding of the molecular genetics of phage infectivity has helped to explain the complex phenotypic coevolutionary dynamics in this system.
84295380
Predation and resource fluctuations drive eco-evolutionary dynamics of a bacterial community
Predation and temporal resource availability are among the most important factors determining prey community dynamics and composition. Both factors have been shown to affect prey diversity, but less is known about their interactive effects, especially in rapidly evolving prey communities. In a laboratory microcosm experiment, we manipulated the presence of the predatory protozoan Tetrahymena thermophila and the temporal patterns in the availability of resources for a bacterial prey community. We found that both predation and temporal fluctuations in prey resources resulted in a more even prey community, and these factors also interacted so that the effect of predation was only seen in a fluctuating environment. One possible explanation for this finding could be differences in prey species grazing resistance and resource use abilities, which likely had the greatest effect on prey community structure in fluctuating environments with periodical resource limitation. We also found that prey communities evolved to be more grazing-resistant during the experiment, and that this effect was due to a clear increase in the grazing resistance of the bacterium Serratia marcescens. Our results demonstrate that temporal variability in prey resources and predation can promote more even prey species proportions by allowing the existence of both defensive and competitive prey life-history strategies.
21612229
Coevolution Drives Temporal Changes in Fitness and Diversity Across Environments in a Bacteria–Bacteriophage Interaction
Abstract Coevolutionary interactions are thought to play a crucial role in diversification of hosts and parasitoids. Furthermore, resource availability has been shown to be a fundamental driver of species diversity. Yet, we still do not have a clear understanding of how resource availability mediates the diversity generated by coevolution between hosts and parasitoids over time. We used experiments with bacteria and bacteriophage to test how resources affect variation in the competitive ability of resistant hosts and temporal patterns of diversity in the host and parasitoid as a result of antagonistic coevolution. Bacteria and bacteriophage coevolved for over 150 bacterial generations under high and low-resource conditions. We measured relative competitive ability of the resistant hosts and phenotypic diversity of hosts and parasitoids after the initial invasion of resistant mutants and again at the end of the experiment. Variation in relative competitive ability of the hosts was both time- and environment-dependent. The diversity of resistant hosts, and the abundance of host-range mutants attacking these phenotypes, differed among environments and changed over time, but the direction of these changes differed between the host and parasitoid. Our results demonstrate that patterns of fitness and diversity resulting from coevolutionary interactions can be highly dynamic.
41049511
Temporal dynamics of antagonism and mutualism in a geographically variable plant-insect interaction.
Variation among sites and years in the local ecological outcome of interspecific interactions can generate a geographic mosaic of coevolution, as indicated by recent mathematical models. We evaluated whether local temporal dynamics of ecological outcome in the interaction between the moth Greya politella (Prodoxidae) and its host plant Lithophragma parviflorum (Saxifragaceae) are likely to mitigate or magnify geographic differences in ecological outcome found in earlier studies. The moths are highly host-specific pollinating floral parasites, and the mutualism can be swamped in some populations by the presence of effective co-pollinators. Hence, differing community contexts can shift the outcome of the interaction from mutualism to commensalism or antagonism. During each of four years, we evaluated the effect of Greya oviposition on seed development through a paired design that controlled for plant genotype and microenvironment. At Turnbull National Wildlife Refuge in Washington State, the interaction was significantly mutualistic in all four years. Mutualism in this population was indicated by a higher probability of development of capsules visited by ovipositing Greya than capsules not visited by Greya on the same plant. At Rapid River, Idaho, the interaction was commensalistic in three years and antagonistic in one year. Antagonism in this population was indicated by selective withering of capsules containing Greya eggs. Overall, the results suggest stable geographic differences in the range of ecological outcomes in this plant-insect interaction under different community contexts.
7319144
COEVOLUTION BETWEEN HISPANIOLAN CROSSBILLS AND PINE: DOES MORE TIME ALLOW FOR GREATER PHENOTYPIC ESCALATION AT LOWER LATITUDE?
Abstract Crossbills (Aves: Loxia) and several conifers have coevolved in predator–prey arms races over the last 10,000 years. However, the extent to which coevolutionary arms races have contributed to the adaptive radiation of crossbills or to any other adaptive radiation is largely unknown. Here we extend our previous studies of geographically structured coevolution by considering a crossbill–conifer interaction that has persisted for a much longer time period and involves a conifer with more variable annual seed production. We examined geographic variation in the cone and seed traits of two sister species of pines, Pinus occidentalis and P. cubensis, on the islands of Hispaniola and Cuba, respectively. We also compared the Hispaniolan crossbill (Loxia megaplaga) to its sister taxa the North American white-winged crossbill (Loxia leucoptera leucoptera). The Hispaniolan crossbill is endemic to Hispaniola whereas Cuba lacks crossbills. In addition and in contrast to previous studies, the variation in selection experienced by these pines due to crossbills is not confounded by the occurrence of selection by tree squirrels (Tamiasciurus and Sciurus). As predicted if P. occidentalis has evolved defenses in response to selection exerted by crossbills, cones of P. occidentalis have scales that are 53% thicker than those of P. cubensis. Cones of P. occidentalis, but not P. cubensis, also have well-developed spines, a known defense against vertebrate seed predators. Consistent with patterns of divergence seen in crossbills coevolving locally with other conifers, the Hispaniolan crossbill has evolved a bill that is 25% deeper than the white-winged crossbill. Together with phylogenetic analyses, our results suggest that predator–prey coevolution between Hispaniolan crossbills and P. occidentalis over approximately 600,000 years has caused substantial morphological evolution in both the crossbill and pine. This also indicates that cone crop fluctuations do not prevent crossbills and conifers from coevolving. Furthermore, because the traits at the phenotypic interface of the interaction apparently remain the same over at least several hundred thousand years, divergence as a result of coevolution is greater at lower latitude where crossbill–conifer interactions have been less interrupted by Pleistocene events.
20903399
Imbalance of Predator and Prey Armament: Geographic Clines in Phenotypic Interface and Natural Selection
The escalation of defensive/offensive arms is ubiquitous in prey‐predator evolutionary interactions. However, there may be a geographically varying imbalance in the armaments of participating species that affects the outcome of local interactions. In a system involving the Japanese camellia (Camellia japonica) and its obligate seed predator, the camellia weevil (Curculio camelliae), we investigated the geographic variation in physical defensive/offensive traits and that in natural selection on the plant’s defense among 17 populations over a 700‐km‐wide area in Japan. The sizes of the plant defensive apparatus (pericarp thickness) and the weevil offensive apparatus (rostrum length) clearly correlated with each other across populations. Nevertheless, the balance in armaments between the two species was geographically structured. In the populations for which the balance was relatively advantageous for the plant’s defense, natural selection on the trait was stronger because in the other populations, most plant individuals were too vulnerable to resist the attacks of the weevil, and their seeds were infested independent of pericarp thickness. We also found that the imbalance between the defensive/offensive armaments and the intensity of natural selection showed clear latitudinal clines. Overall, our results suggest that the imbalance of armament between sympatric prey and predator could determine the strength of local selection and that climatic conditions could affect the local and overall trajectory of coevolutionary arms races.
1763025
Coevolution between crossbills and black pine: the importance of competitors, forest area and resource stability
Studies of predator‐prey interactions have found that geographically structured coevolution has played an important role in the adaptive diversification of crossbills (Loxia spp.). We extend those studies by considering common crossbills (L. curvirostra) in the Mediterranean where they rely on seeds in the cones of black pine (Pinus nigra). On the continent, where tree squirrels (Sciurus vulgaris) are present, enhanced defenses against crossbills were most evident in larger areas of pine forest. On islands in the absence of tree squirrels, crossbills and black pine have coevolved in a predator‐prey arms race on Cyprus but not Corsica. In contrast to other conifers that island endemic crossbills rely upon, black pine does not hold seeds in its cones year round. Consequently, key to the strong crossbill–pine interaction on Cyprus is likely the presence of an alternative conifer that provides seeds during early summer when black pine seeds are scarce.