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.     

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.     

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.     

The maintenance of genetic diversity under host–parasite coevolution in finite,structured populations

As a corollary to the Red Queen hypothesis, host–parasite coevolution has been hypothesized to maintain genetic variation in both species. Recent theoretical work, however, suggests that reciprocal natural selection alone is insufficient to maintain variation at individual loci. As highlighted by our brief review of the theoretical literature, models of host–parasite coevolution often vary along multiple axes (e.g. inclusion of ecological feedbacks or abiotic selection mosaics), complicating a comprehensive understanding of the effects of interacting evolutionary processes on diversity. Here we develop a series of comparable models to explore the effect of interactions between spatial structures and antagonistic coevolution on genetic diversity. Using a matching alleles model in finite populations connected by migration, we find that, in contrast to panmictic populations, coevolution in a spatially structured environment can maintain genetic variation relative to neutral expectations with migration alone. These results demonstrate that geographic structure is essential for understanding the effect of coevolution on biological diversity.     

The potential of a population genomics approach to analyse geographic mosaics of plant--insect coevolution

A central issue in the evolutionary ecology of species interactions is coevolution, which involves the reciprocal selection between individuals of interacting species. Understanding the importance of coevolution in shaping species interactions requires the consideration of spatial variation in their strength. This is exactly what the, recently developed, geographic mosaic theory of coevolution addresses. Another major development in the study of population ecology is the introduction of the population genomics approach in this field of research. This approach addresses spatial processes through molecular methods. It is of particular interest that population genomics is especially applicable to natural populations of non-model species. We describe how population genomics can be used in the context of the geographic mosaic of coevolution, specifically to identify coevolutionary hot-spots, and to attribute genetic variation found at specific loci to processes of selection versus trait remixing. The proposed integration of the population genomics approach with the conceptual framework of the geographic mosaic of coevolution is illustrated with a few selected, particularly demonstrative, examples from the realm of insect--plant interactions.     

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.     

The ecology and evolution of host-plant resistance to insects

Genetic techniques have yielded new insights into plant-herbivore coevolution. Quantitative genetic tests of herbivory theory reveal that in some cases insect herbivores impose selection on resistance traits. Also, some resistance traits are costly while others appear not to be, and genetic models can explain these results. Genetic variation in plant resistance influences insect community structure by modifying interactions of herbivores with competitors and natural enemies. Therefore, models of multispecies coevolution are more realistic than pairwise coevolutionary models. Ecological genetics will facilitate further theoretical and empirical exploration of multispecies coevolution of plants and herbivores.     

Genetic dimension of the coevolution of virulence-resistance in Drosophila -- parasitoid wasp relationships

Variations observed in parasite virulence and host resistance may be the outcome of coevolutionary processes. Recent theoretical developments have led to a 'geographic mosaic theory' of coevolution according to which there are some localities where reciprocal selection occurs (hot spots) and others where it is strongly reduced (cold spots). Studies of host-parasitoid systems back this up, revealing a geographical variation of traits subjected to antagonistic selection governed by variations in the strength of the ecological interactions. A more detailed analysis of the genetic basis of these geographic variations in a model system -- the interaction between Drosophila melanogaster and its specific parasitoid Leptopilina boulardi -- suggests that cold spots and hot spots are also driven by the amount of genetic variation available for the trait considered. Our approach, based on isolating reference strains, has been found to predict the result of sympatric interactions and it will be helpful in identifying the selective forces responsible for the coevolution. In this model, host resistance to a standardised reference strain is a weak predictor of the outcome of interactions in the field, and the main parameter accounting for the geographic variations is the number of host species available, with less parasitoid virulence towards D. melanogaster being found in areas displaying a more diversified host community.     

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.     

Sensory exploitation and sexual conflict

Much of the literature on male-female coevolution concerns the processes by which male traits and female preferences for these can coevolve and be maintained by selection. There has been less explicit focus on the origin of male traits and female preferences. Here, I argue that it is important to distinguish origin from subsequent coevolution and that insights into the origin can help us appreciate the relative roles of various coevolutionary processes for the evolution of diversity in sexual dimorphism. I delineate four distinct scenarios for the origin of male traits and female preferences that build on past contributions, two of which are based on pre-existing variation in quality indicators among males and two on exploitation of pre-existing sensory biases among females. Recent empirical research, and theoretical models, suggest that origin by sensory exploitation has been widespread. I argue that this points to a key, but perhaps transient, role for sexually antagonistic coevolution (SAC) in the subsequent evolutionary elaboration of sexual traits, because (i) sensory exploitation is often likely to be initially costly for individuals of the exploited sex and (ii) the subsequent evolution of resistance to sensory exploitation should often be associated with costs due to selective constraints. A review of a few case studies is used to illustrate these points. Empirical data directly relevant to the costs of being sensory exploited and the costs of evolving resistance is largely lacking, and I stress that such data would help determining the general importance of sexual conflict and SAC for the evolution of sexual dimorphism.     

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.     

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.     

Balancing Selection for Pathogen Resistance Reveals an Intercontinental Signature of Red Queen Coevolution

The link between long-term host–parasite coevolution and genetic diversity is key to understanding genetic epidemiology and the evolution of resistance. The model of Red Queen host–parasite coevolution posits that high genetic diversity is maintained when rare host resistance variants have a selective advantage, which is believed to be the mechanistic basis for the extraordinarily high levels of diversity at disease-related genes such as the major histocompatibility complex in jawed vertebrates and R-genes in plants. The parasites that drive long-term coevolution are, however, often elusive. Here we present evidence for long-term balancing selection at the phenotypic (variation in resistance) and genomic (resistance locus) level in a particular host–parasite system: the planktonic crustacean Daphnia magna and the bacterium Pasteuria ramosa. The host shows widespread polymorphisms for pathogen resistance regardless of geographic distance, even though there is a clear genome-wide pattern of isolation by distance at other sites. In the genomic region of a previously identified resistance supergene, we observed consistent molecular signals of balancing selection, including higher genetic diversity, older coalescence times, and lower differentiation between populations, which set this region apart from the rest of the genome. We propose that specific long-term coevolution by negative-frequency-dependent selection drives this elevated diversity at the host''s resistance loci on an intercontinental scale and provide an example of a direct link between the host’s resistance to a virulent pathogen and the large-scale diversity of its underlying genes.     

The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts

The "geographic mosaic" approach to understanding coevolution is predicated on the existence of variable selection across the landscape of an interaction between species. A range of ecological factors, from differences in resource availability to differences in community composition, can generate such a mosaic of selection among populations, and thereby differences in the strength of coevolution. The result is a mixture of hotspots, where reciprocal selection is strong, and coldspots, where reciprocal selection is weak or absent, throughout the ranges of species. Population subdivision further provides the opportunity for nonadaptive forces, including gene flow, drift, and metapopulation dynamics, to influence the coevolutionary interaction between species. Some predicted results of this geographic mosaic of coevolution include maladapted or mismatched phenotypes, maintenance of high levels of polymorphism, and prevention of stable equilibrium trait combinations. To evaluate the potential for the geographic mosaic to influence predator-prey coevolution, we investigated the geographic pattern of genetically determined TTX resistance in the garter snake Thamnophis sirtalis over much of the range of its ecological interaction with toxic newts of genus Taricha. We assayed TTX resistance in over 2900 garter snakes representing 333 families from 40 populations throughout western North America. Our results provide dramatic evidence that geographic structure is an important component in coevolutionary interactions between predators and prey. Resistance levels vary substantially (over three orders of magnitude) among populations and over short distances. The spatial array of variation is consistent with two areas of intense evolutionary response by predators ("hotspots") surrounded by clines of decreasing resistance. Some general predictions of the geographic mosaic process are supported, including clinal variation in phenotypes, polymorphism in some populations, and divergent outcomes of the interaction between predator and prey. Conversely, our data provide little support for one of the major predictions, mismatched values of interacting traits. Two lines of evidence suggest selection is paramount in determining population variation in resistance. First, phylogenetic information indicates that two hotspots of TTX resistance have evolved independently. Second, in the one region that TTX levels in prey have been quantified, resistance and toxicity levels match almost perfectly over a wide phenotypic and geographic range. However, these results do not preclude the role the nonadaptive forces in generating the overall geographic mosaic of TTX resistance. Much work remains to fill in the geographic pattern of variation among prey populations and, just as importantly, to explore the variation in the ecology of the interaction that occurs within populations.     

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 SBW25Phi2. 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.     

The coevolutionary dynamics of antagonistic interactions mediated by quantitative traits with evolving variances

Quantitative traits frequently mediate coevolutionary interactions between predator and prey or parasite and host. Previous efforts to understand and predict the coevolutionary dynamics of these interactions have generally assumed that standing genetic variation is fixed or absent altogether. We develop a genetically explicit model of coevolution that bridges the gap between these approaches by allowing genetic variation itself to evolve. Analysis of this model shows that the evolution of genetic variance has important consequences for the dynamics and outcome of coevolution. Of particular importance is our demonstration that coevolutionary cycles can emerge in the absence of stabilizing selection, an outcome not possible in previous models of coevolution mediated by quantitative traits. Whether coevolutionary cycles evolve depends upon the strength of selection, the number of loci, and the rate of mutation in each of the interacting species. Our results also generate novel predictions for the expected sign and magnitude of linkage disequilibria in each species.     

Plasmid carriage can limit bacteria–phage coevolution

Coevolution with bacteriophages is a major selective force shaping bacterial populations and communities. A variety of both environmental and genetic factors has been shown to influence the mode and tempo of bacteria–phage coevolution. Here, we test the effects that carriage of a large conjugative plasmid, pQBR103, had on antagonistic coevolution between the bacterium Pseudomonas fluorescens and its phage, SBW25ϕ2. Plasmid carriage limited bacteria–phage coevolution; bacteria evolved lower phage-resistance and phages evolved lower infectivity in plasmid-carrying compared with plasmid-free populations. These differences were not explained by effects of plasmid carriage on the costs of phage resistance mutations. Surprisingly, in the presence of phages, plasmid carriage resulted in the evolution of high frequencies of mucoid bacterial colonies. Mucoidy can provide weak partial resistance against SBW25ϕ2, which may have limited selection for qualitative resistance mutations in our experiments. Taken together, our results suggest that plasmids can have evolutionary consequences for bacteria that go beyond the direct phenotypic effects of their accessory gene cargo.     

Two-step infection processes can lead to coevolution between functionally independent infection and resistance pathways

There is growing evidence that successful infection of hosts by pathogens requires a series of independent steps. However, how multistep infection processes affect host-pathogen coevolution is unclear. We present a coevolutionary model, inspired by empirical observations from a range of host-pathogen systems, where the infection process consists of the following two steps: the first is for the pathogen to recognize and locate a suitable host, and the second is to exploit the host while evading immunity. Importantly, these two steps conform to different models of infection genetics: inverse-gene-for-gene (IGFG) and gene-for-gene (GFG), respectively. We show that coevolution under this scenario can lead to coupled gene frequency changes across these two systems. In particular, selection often favors pathogens that are infective at the first, IGFG, step and hosts that are resistant at the second, GFG, step. Hence, there may be signals of positive selection between functionally independent systems whenever there are multistep processes determining resistance and infectivity. Such multistep infection processes are a fundamental, but overlooked feature of many host-pathogen interactions, and have important consequences for our understanding of host-pathogen coevolution.     

EXPERIMENTAL MANIPULATION OF PUTATIVE SELECTIVE AGENTS PROVIDES EVIDENCE FOR THE ROLE OF NATURAL ENEMIES IN THE EVOLUTION OF PLANT DEFENSE

Although biologists have long assumed that plant resistance characters evolved under selection exerted by such natural enemies as herbivores and pathogens, experimental evidence for this assumption is sparse. We present evidence that natural enemies exert selection on particular plant resistance characters. Specifically, we demonstrate that elimination of natural enemies from an experimental field population of Arabidopsis thaliana alters the pattern of selection on genetic variation in two characters that have been shown to reduce herbivore damage in the field: total glucosinolate concentration and trichome density. The change in pattern of selection reveals that natural enemies imposed selection favoring increased glucosinolate concentration and increased trichome density, and thus, supports one of the major assumptions of the coevolution hypothesis. We also demonstrate that a pattern of stabilizing selection on glucosinolate concentration results from a balance between the costs and benefits associated with increasing levels of this resistance character. This result provides direct confirmation of the appropriateness of cost-benefit models for characterizing the evolution of plant defenses.     

Red queen meets Santa Rosalia: arms races and the evolution of host specialization in organisms with parasitic lifestyles

I argue that nonequilibrium allele frequency dynamics due to coevolution can drive the evolution of specialized host races in parasites capable of host choice-for example, herbivorous insects or parasitoids. The proposed mechanism does not require genetic trade-offs in performance on different host species. It is based on the premise that the ability of the parasite to overcome the resistance of different host species is to a large degree genetically independent-that is, controlled by different loci. The intuitive rationale is that the genetic lineage of a parasite that evolves host preference becomes more consistently exposed to selection for performance on its preferred host. Such a choosy lineage can thus coevolve faster in response to evolving host defenses than a generalist lineage distributed among several host species. Given genetic variation in host preference, an initially generalist parasite population evolves toward specialized host races, each choosing one host species. This idea is supported by a series of multilocus models of coevolution between a parasite and two host species, in which the parasite virulence on each host is affected by a different set of loci and an additional locus or two loci control host choice.