HOW DOES SPATIAL DISPERSAL NETWORK AFFECT THE EVOLUTION OF PARASITE LOCAL ADAPTATION?

Studying patterns of parasite local adaptation can provide insights into the spatiotemporal dynamics of host–parasite coevolution. Many factors, both biotic and abiotic, have been identified that influence parasite local adaptation. In particular, dispersal and population structuring are considered important determinants of local adaptation. We investigated how the shape of the spatial dispersal network within experimental landscapes affected local adaptation of a bacteriophage parasite to its bacterial host. Regardless of landscape topology, dispersal always led to the evolution of phages with broader infectivity range. However, when the spatial dispersal network resulted in spatial variation in the breadth of phage infectivity range, significant levels of parasite local adaptation and local maladaptation were detected within the same landscape using the local versus foreign definition of local adaptation. By contrast, local adaptation was not detected using the home versus away or local versus global definitions of local adaptation. This suggests that spatial dispersal networks may play an important role in driving parasite local adaptation, particularly when the shape of the dispersal network generates nonuniform levels of host resistance or parasite infectivity throughout a species’ range.     

Bacterial cell‐to‐cell signaling promotes the evolution of resistance to parasitic bacteriophages

The evolution of host–parasite interactions could be affected by intraspecies variation between different host and parasite genotypes. Here we studied how bacterial host cell‐to‐cell signaling affects the interaction with parasites using two bacteria‐specific viruses (bacteriophages) and the host bacterium Pseudomonas aeruginosa that communicates by secreting and responding to quorum sensing (QS) signal molecules. We found that a QS‐signaling proficient strain was able to evolve higher levels of resistance to phages during a short‐term selection experiment. This was unlikely driven by demographic effects (mutation supply and encounter rates), as nonsignaling strains reached higher population densities in the absence of phages in our selective environment. Instead, the evolved nonsignaling strains suffered relatively higher growth reduction in the absence of the phage, which could have constrained the phage resistance evolution. Complementation experiments with synthetic signal molecules showed that the Pseudomonas quinolone signal (PQS) improved the growth of nonsignaling bacteria in the presence of a phage, while the activation of las and rhl quorum sensing systems had no effect. Together, these results suggest that QS‐signaling can promote the evolution of phage resistance and that the loss of QS‐signaling could be costly in the presence of phages. Phage–bacteria interactions could therefore indirectly shape the evolution of intraspecies social interactions and PQS‐mediated virulence in P. aeruginosa.     

Spatial heterogeneity and the stability of host-parasite coexistence

Spatially heterogeneous environments can theoretically promote more stable coexistence of hosts and parasites by reducing the risk of parasite attack either through providing permanent spatial refuges or through providing ephemeral refuges by reducing dispersal. In experimental populations of Pseudomonas aeruginosa and the bacteriophage PP7, spatial heterogeneity promoted stable coexistence of host and parasite, while coexistence was significantly less stable in the homogeneous environment. Phage populations were found to be persisting on subpopulations of sensitive bacteria. Transferring populations to fresh microcosms every 24 h prevented the development of permanent spatial refuges. However, the lower dispersal rates in the heterogeneous environment were found to reduce parasite transmission thereby creating ephemeral refuges from phage attack. These results suggest that spatial heterogeneity can stabilize an otherwise unstable host-parasite interaction even in the absence of permanent spatial refuges.     

Spatial heterogeneity lowers rather than increases host–parasite specialization

Abiotic environmental heterogeneity can promote the evolution of diverse resource specialists, which in turn may increase the degree of host–parasite specialization. We coevolved Pseudomonas fluorescens and lytic phage ?2 in spatially structured populations, each consisting of two interconnected subpopulations evolving in the same or different nutrient media (homogeneous and heterogeneous environments, respectively). Counter to the normal expectation, host–parasite specialization was significantly lower in heterogeneous compared with homogeneous environments. This result could not be explained by dispersal homogenizing populations, as this would have resulted in the heterogeneous treatments having levels of specialization equal to or greater than that of the homogeneous environments. We argue that selection for costly generalists is greatest when the coevolving species are exposed to diverse environmental conditions and that this can provide an explanation for our results. A simple coevolutionary model of this process suggests that this can be a general mechanism by which environmental heterogeneity can reduce rather than increase host–parasite specialization.     

Parasite host range and the evolution of host resistance

Parasite host range plays a pivotal role in the evolution and ecology of hosts and the emergence of infectious disease. Although the factors that promote host range and the epidemiological consequences of variation in host range are relatively well characterized, the effect of parasite host range on host resistance evolution is less well understood. In this study, we tested the impact of parasite host range on host resistance evolution. To do so, we used the host bacterium Pseudomonas fluorescens SBW25 and a diverse suite of coevolved viral parasites (lytic bacteriophage Φ2) with variable host ranges (defined here as the number of host genotypes that can be infected) as our experimental model organisms. Our results show that resistance evolution to coevolved phages occurred at a much lower rate than to ancestral phage (approximately 50% vs. 100%), but the host range of coevolved phages did not influence the likelihood of resistance evolution. We also show that the host range of both single parasites and populations of parasites does not affect the breadth of the resulting resistance range in a naïve host but that hosts that evolve resistance to single parasites are more likely to resist other (genetically) more closely related parasites as a correlated response. These findings have important implications for our understanding of resistance evolution in natural populations of bacteria and viruses and other host–parasite combinations with similar underlying infection genetics, as well as the development of phage therapy.     

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.     

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.     

Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria‐phage system

Host–parasite evolutionary interactions are typically considered in a pairwise species framework. However, natural infections frequently involve multiple parasites. Altering parasite diversity alters ecological and evolutionary dynamics as parasites compete and hosts resist multiple infection. We investigated the effects of parasite diversity on host–parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites. To manipulate parasite diversity, bacterial populations were exposed for 24 hours to either phage monocultures or diverse communities containing up to five phages. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to interphage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. We observed no difference in the extent of resistance with increased parasite diversity, but there was a profound impact on the specificity of resistance; specialized resistance evolved to monocultures through mutations in a diverse set of genes. In summary, we demonstrate that parasite diversity has rapid effects on host–parasite population dynamics and evolution by selecting for different resistance mutations and affecting the magnitude of bacterial suppression and recovery. Finally, we discuss the implications of phage diversity for their use as biological control agents.     

Modification of the interaction betweenEscherichia coli and bacteriophage in saline sediment

The effects of sorption phenomena on the interaction between a parasite and its host bacterium have been investigated using anEscherichia coli-bacteriophage-saline sediment system. The sediment contained organic matter and a high proportion of clay, predominantly montmorillonoid. BothE. coli and phage remained firmly sorbed to saline sediments or montmorillonite, but were rapidly desorbed following dilution of the electrolyte below a critical concentration. This desorption coincided with the dispersal of sediment colloids.Escherichia coli was protected from phage attack by the presence of sediment, montmorillonite, or organic matter at salinty levels both above and below this critical point for dispersal and desorption. Evidence is presented indicating thatE. coli is protected from phage attack at low electrolyte concentrations by an envelope of sorbed colloidal materials around the cell, whereas at high electrolyte concentrations protection results both from the colloid envelope around the cells as well as from the sorption of cells and phages to solid particles. The protection ofE. coli and possibly other fecal bacteria may result in their accumulation in saline sediments, producing a possible health hazard in estuaries and lagoons if the bacteria are desorbed following dilution as a result of heavy rainfall.     

Dispersal network structure and infection mechanism shape diversity in a coevolutionary bacteria-phage system

Resource availability, dispersal and infection genetics all have the potential to fundamentally alter the coevolutionary dynamics of bacteria–bacteriophage interactions. However, it remains unclear how these factors synergise to shape diversity within bacterial populations. We used a combination of laboratory experiments and mathematical modeling to test how the structure of a dispersal network affects host phenotypic diversity in a coevolving bacteria-phage system in communities of differential resource input. Unidirectional dispersal of bacteria and phage from high to low resources consistently increased host diversity compared with a no dispersal regime. Bidirectional dispersal, on the other hand, led to a marked decrease in host diversity. Our mathematical model predicted these opposing outcomes when we incorporated modified gene-for-gene infection genetics. To further test how host diversity depended on the genetic underpinnings of the bacteria-phage interaction, we expanded our mathematical model to include different infection mechanisms. We found that the direction of dispersal had very little impact on bacterial diversity when the bacteria-phage interaction was mediated by matching alleles, gene-for-gene or related infection mechanisms. Our experimental and theoretical results demonstrate that the effects of dispersal on diversity in coevolving host–parasite systems depend on an intricate interplay of the structure of the underlying dispersal network and the specifics of the host–parasite interaction.     

Local biotic environment shapes the spatial scale of bacteriophage adaptation to bacteria

The ecological, epidemiological, and evolutionary consequences of host-parasite interactions are critically shaped by the spatial scale at which parasites adapt to hosts. The scale of interaction between hyperparasites and their parasites is likely to be influenced by the host of the parasite and potentially likely to differ among within-host environments. Here we examine the scale at which bacteriophages adapt to their host bacteria by studying natural isolates from the surface or interior of horse chestnut leaves. We find that phages are more infective to bacteria from the same tree relative to those from other trees but do not differ in infectivity to bacteria from different leaves within the same tree. The results suggest that phages target common bacterial species, including an important plant pathogen, within plant host tissues; this result has important implications for therapeutic phage epidemiology. Furthermore, we show that phages from the leaf interior are more infective to their local hosts than phages from the leaf surface are to theirs, suggesting either increased resistance of bacteria on the leaf surface or increased phage adaptation within the leaf. These results highlight that biotic environment can play a key role in shaping the spatial scale of parasite adaptation and influencing the outcome of coevolutionary interactions.     

Diversity in CRISPR‐based immunity protects susceptible genotypes by restricting phage spread and evolution

Diversity in host resistance often associates with reduced pathogen spread. This may result from ecological and evolutionary processes, likely with feedback between them. Theory and experiments on bacteria–phage interactions have shown that genetic diversity of the bacterial adaptive immune system can limit phage evolution to overcome resistance. Using the CRISPR–Cas bacterial immune system and lytic phage, we engineered a host–pathogen system where each bacterial host genotype could be infected by only one phage genotype. With this model system, we explored how CRISPR diversity impacts the spread of phage when they can overcome a resistance allele, how immune diversity affects the evolution of the phage to increase its host range and if there was feedback between these processes. We show that increasing CRISPR diversity benefits susceptible bacteria via a dilution effect, which limits the spread of the phage. We suggest that this ecological effect impacts the evolution of novel phage genotypes, which then feeds back into phage population dynamics.     

Evolution of spatially structured host–parasite interactions

Spatial structure has dramatic effects on the demography and the evolution of species. A large variety of theoretical models have attempted to understand how local dispersal may shape the coevolution of interacting species such as host–parasite interactions. The lack of a unifying framework is a serious impediment for anyone willing to understand current theory. Here, we review previous theoretical studies in the light of a single epidemiological model that allows us to explore the effects of both host and parasite migration rates on the evolution and coevolution of various life‐history traits. We discuss the impact of local dispersal on parasite virulence, various host defence strategies and local adaptation. Our analysis shows that evolutionary and coevolutionary outcomes crucially depend on the details of the host–parasite life cycle and on which life‐history trait is involved in the interaction. We also discuss experimental studies that support the effects of spatial structure on the evolution of host–parasite interactions. This review highlights major similarities between some theoretical results, but it also reveals an important gap between evolutionary and coevolutionary models. We discuss possible ways to bridge this gap within a more unified framework that would reconcile spatial epidemiology, evolution and coevolution.     

Strong dispersal in a parasitoid wasp overwhelms habitat fragmentation and host population dynamics

The population dynamics of a parasite depend on species traits, host dynamics and the environment. Those dynamics are reflected in the genetic structure of the population. Habitat fragmentation has a greater impact on parasites than on their hosts because resource distribution is increasingly fragmented for species at higher trophic levels. This could lead to either more or less genetic structure than the host, depending on the relative dispersal rates of species. We examined the spatial genetic structure of the parasitoid wasp Hyposoter horticola, and how it was influenced by dispersal, host population dynamics and habitat fragmentation. The host, the Glanville fritillary butterfly, lives as a metapopulation in a fragmented landscape in the Åland Islands, Finland. We collected wasps throughout the 50 by 70 km archipelago and determined the genetic diversity, spatial population structure and genetic differentiation using 14 neutral DNA microsatellite loci. We compared the genetic structure of the wasp with that of the host butterfly using published genetic data collected over the shared landscape. Using maternity assignment, we also identified full‐siblings among the sampled parasitoids to estimate the dispersal range of individual females. We found that because the parasitoid is dispersive, it has low genetic structure, is not very sensitive to habitat fragmentation and has less spatial genetic structure than its butterfly host. The wasp is sensitive to regional rather than local host dynamics, and there is a geographic mosaic landscape for antagonistic co‐evolution of host resistance and parasite virulence.     

Weak link between dispersal and parasite community differentiation or immunogenetic divergence in two sympatric cichlid fishes

Geographical isolation, habitat variation and trophic specialization have contributed to a large extent to the astonishing diversity of cichlid fishes in the Great East African lakes. Because parasite communities often vary across space and environments, parasites can accompany and potentially enhance cichlid species diversification. However, host dispersal may reduce opportunities for parasite‐driven evolution by homogenizing parasite communities and allele frequencies of immunity genes. To test for the relationships between parasite community variation, host dispersal and parasite‐induced host evolution, we studied two sympatric cichlid species with contrasting dispersal capacities along the shores of southern Lake Tanganyika. Whereas the philopatric Tropheus moorii evolved into several genetically differentiated colour morphs, Simochromis diagramma is phenotypically rather uniform across its distribution range and shows only weak population structure. Populations of both species were infected with divergent parasite communities and harbour differentiated variant pools of an important set of immune genes, the major histocompatibility complex (MHC). The overall extent of geographical variation of parasites and MHC genes was similar between host species. This indicates that immunogenetic divergence among populations of Lake Tanganyika cichlids can occur even in species that are strongly dispersing. However, because this also includes species that are phenotypically uniform, parasite‐induced evolution may not represent a key factor underlying species diversification in this system.     

The evolution of bacterial resistance against bacteriophages in the horse chestnut phyllosphere is general across both space and time

Insight to the spatial and temporal scales of coevolution is key to predicting the outcome of host–parasite interactions and spread of disease. For bacteria infecting long-lived hosts, selection to overcome host defences is just one factor shaping the course of evolution; populations will also be competing with other microbial species and will themselves be facing infection by bacteriophage viruses. Here, we examine the temporal and spatial patterns of bacterial adaptation against natural phage populations from within leaves of horse chestnut trees. Using a time-shift experiment with both sympatric and allopatric phages from either contemporary or earlier points in the season, we demonstrate that bacterial resistance is higher against phages from the past, regardless of spatial sympatry or how much earlier in the season phages were collected. Similarly, we show that future bacterial hosts are more resistant to both sympatric and allopatric phages than contemporary bacterial hosts. Together, our results suggest the evolution of relatively general bacterial resistance against phages in nature and are contrasting to previously observed patterns of phage adaptation to bacteria from the same tree hosts over the same time frame, indicating a potential asymmetry in coevolutionary dynamics.     

How parasite-mediated costs drive the evolution of disease state-dependent dispersal

The process of dispersal is central to population biology and evolutionary ecology. Because of negative impacts on host fitness, parasite infection generates potential costs of dispersal. However, theoretical predictions that address this issue are lacking. Here, we develop a mathematical model to demonstrate how the dispersal rate of hosts evolves under the influence of parasites in ecological scenarios incorporating pre-, during-, and post-dispersal infection/recovery events. We show that (1) the dispersal tendency is strongly biased towards either infected individuals or susceptible individuals, (2) the bias is inherently determined by the parasite-mediated relative cost of dispersal, and (3) the dispersal costs are determined by the autocorrelation of disease states (susceptible and infected) between pre- and post-dispersal. Our results suggest that parasite virulence in concert with the timing of infection drive the evolution of disease state-biased dispersal. To understand the evolutionary processes in spatial host–parasite systems, the parasite-induced costs of dispersal need to be taken into account.     

SELECTION OF BENEVOLENCE IN A HOST–PARASITE SYSTEM

A paradigm for the evolution of cooperation between parasites and their hosts argues that the mode of parasite transmission is critical to the long-term maintenance of cooperation. Cooperation is not expected to be maintained whenever the chief mode of transmission is horizontal: a parasite's progeny infect hosts unrelated to their parent's host. Cooperation is expected to be maintained if the chief mode of transmission is vertical: a parasite's progeny infect only the parent's host or descendants of that host. This paradigm was tested using bacteria and filamentous bacteriophage (f1). When cells harboring different variants of these phage were cultured so that no infectious spread was allowed, ensuring that all parasite transmission was vertical, selection favored the variants that were most benevolent to the host—those that least harmed host growth rate. By changing the culture conditions so that horizontal spread of the phage was allowed, the selective advantage of the benevolent forms was lost. These experiments thus support the theoretical arguments that mode of transmission is a major determinant in the evolution of cooperation between a parasite and its host.     

Host dispersal as the driver of parasite genetic structure: a paradigm lost?

Understanding traits influencing the distribution of genetic diversity has major ecological and evolutionary implications for host–parasite interactions. The genetic structure of parasites is expected to conform to that of their hosts, because host dispersal is generally assumed to drive parasite dispersal. Here, we used a meta‐analysis to test this paradigm and determine whether traits related to host dispersal correctly predict the spatial co‐distribution of host and parasite genetic variation. We compiled data from empirical work on local adaptation and host–parasite population genetic structure from a wide range of taxonomic groups. We found that genetic differentiation was significantly lower in parasites than in hosts, suggesting that dispersal may often be higher for parasites. A significant correlation in the pairwise genetic differentiation of hosts and parasites was evident, but surprisingly weak. These results were largely explained by parasite reproductive mode, the proportion of free‐living stages in the parasite life cycle and the geographical extent of the study; variables related to host dispersal were poor predictors of genetic patterns. Our results do not dispel the paradigm that parasite population genetic structure depends on host dispersal. Rather, we highlight that alternative factors are also important in driving the co‐distribution of host and parasite genetic variation.     

Spatial structure,host heterogeneity and parasite virulence: implications for vaccine‐driven evolution

Natural host‐parasite interactions exhibit considerable variation in host quality, with profound consequences for disease ecology and evolution. For instance, treatments (such as vaccination) may select for more transmissible or virulent strains. Previous theory has addressed the ecological and evolutionary impact of host heterogeneity under the assumption that hosts and parasites disperse globally. Here, we investigate the joint effects of host heterogeneity and local dispersal on the evolution of parasite life‐history traits. We first formalise a general theoretical framework combining variation in host quality and spatial structure. We then apply this model to the specific problem of parasite evolution following vaccination. We show that, depending on the type of vaccine, spatial structure may select for higher or lower virulence compared to the predictions of non‐spatial theory. We discuss the implications of our results for disease management, and their broader fundamental relevance for other causes of host heterogeneity in nature.