Coevolving parasites enhance the diversity-decreasing effect of dispersal

High dispersal rates between patches in spatially structured populations can impede diversification and homogenize diversity. These homogenizing effects of dispersal are likely to be enhanced by coevolving parasites that impose strong selection on hosts for resistance. However, the interactive effects of dispersal and parasites on host diversification have never been tested. We used spatially structured, experimental populations of the bacterium Pseudomonas fluorescens, cultured with or without the phage SBW25Ф2 under three levels of dispersal (none, localized or global), and quantified diversity in terms of evolved bacterial colony morphologies after approximately 100 bacterial generations. We demonstrate that higher levels of colony morphology richness evolved in the presence of phage, and that dispersal reduced diversity most strongly in the presence of phage. Thus, our results suggest that, while parasites can drive host diversification, host populations coevolving with parasites are more prone to homogenization through dispersal.     

Density-dependent habitat selection by brown-headed cowbirds (<Emphasis Type="Italic">Molothrus ater</Emphasis>) in tallgrass prairie

Local distributions of avian brood parasites among their host habitats may depend upon conspecific parasite density. We used isodar analysis to test for density-dependent habitat selection in brown-headed cowbirds (Molothrus ater) among tallgrass prairie adjacent to wooded edges, and prairie interior habitat (>100 m from wooded edges) with and without experimental perches. Eight study sites containing these three habitat treatments were established along a geographical gradient in cowbird abundance within the Flint Hills region of Eastern Kansas and Oklahoma, USA. The focal host species of our study, the dickcissel (Spiza americana), is the most abundant and preferred cowbird host in the prairie of this region. Cowbird relative abundance and cowbird:host abundance ratios were used as estimates of female cowbird density, whereas cowbird egg density was measured as parasitism frequency (percent of dickcissel nests parasitized), and parasitism intensity (number of cowbird eggs per parasitized nest). Geographical variation in cowbird abundance was independent of host abundance. Within study sites, host abundance was highest in wooded edge plots, intermediate in the experimental perch plots, and lowest in prairie interior. Cowbirds exhibited a pattern of density-dependent selection of prairie edge versus experimental perch and interior habitats. On sites where measures of cowbird density were lowest, all cowbird density estimates (female cowbirds and their eggs) were highest near (100 m) wooded edges, where host and perch availability are highest. However, as overall cowbird density increased geographically, these density estimates increased more rapidly in experimental perch plots and prairie interiors. Variation in cowbird abundance and cowbird:host ratios suggested density-dependent cowbird selection of experimental perch over prairie interior habitat, but parasitism levels on dickcissel nests were similar among these two habitats at all levels of local cowbird parasitism. The density-dependent pattern of cowbird distribution among prairie edge and interior suggested that density effects on perceived cowbird fitness are greatest at wooded edges. A positive relationship between daily nest mortality rates of parasitized nests during the nestling period with parasitism intensity levels per nest suggested a density-dependent effect on cowbird reproductive success. However, this relationship was similar among habitats, such that all habitats should have been perceived as being equally suitable to cowbirds at all densities. Other unmeasured effects on cowbird habitat suitability (e.g., reduced cowbird success in edge-dwelling host nests, cowbird despotism at edges) might have affected cowbird habitat selection. Managers attempting to minimize cowbird parasitism on sensitive cowbird hosts should consider that hosts in otherwise less-preferred cowbird habitats (e.g., habitat interiors) are at greater risk of being parasitized where cowbirds become particularly abundant.     

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.     

扩散对破碎化景观上宿主-寄生种群动态的影响

景观破碎化和扩散是空间种群模型的重要因素,对生物入侵存在着深远的影响。本章将基于偶对近似模型,探讨由局部和全局宿主-寄生相互作用共同决定的扩散模式对破坏性景观上疾病入侵与传播的影响。其中,生境破坏由生境丧失量与生境破碎化程度来描述。模拟结果显示,宿主和病毒的全局扩散对疾病的入侵与种群密度产生不对称效应：病毒的全局扩散对系统产生的影响较宿主的全局扩散更为显著。不同扩散模式下,生境丧失越高或破碎化程度越低,均将越有害于寄生病毒的入侵;同时,生境的破坏程度也显著地影响了入侵阈值对扩散模式的响应机制。本文研究结果暗示,景观破碎化的空间分布格局以及病毒扩散的限制均可作为物种保护与管理中有效的疾病控制策略。该研究结果在一定意义上丰富和发展了寄生感染理论,为物种保护提供了生态学理论依据。     

Density-dependent host selection in ectoparasites: An application of isodar theory to fleas parasitizing rodents

Parasites should make the same decisions that every animal makes regarding fitness reward. They can maximize reproductive success by selection of those habitats that guarantee the greatest fitness output. We consider the host population as a habitat of a parasite population. Consequently, hosts (=habitats) that differ quantitatively or qualitatively will support different numbers of parasites. The nature of habitat selection can be detected by isodars, lines along which habitat selection yields equivalent fitness reward. We applied this approach to study host selection of five fleas, each infesting two desert rodents. Xenopsylla conformis, Xenopsylla ramesis, Nosopsyllus iranus theodori and Stenoponia tripectinata medialis parasitize Gerbillus dasyurus and Meriones crassus. Synosternus cleopatrae pyramidis parasitizes Gerbillus andersoni allenbyi and Gerbillus pyramidum. Three fleas ( X. conformis, X. ramesis and S. c. pyramidis) were able to perceive quantitative (amount of the resource; e.g. organic matter in the nest for flea larvae) and/or qualitative (pattern of resource acquisition; e.g. host defensiveness) differences between hosts. Two other fleas did not perceive between-host differences. X. conformis was a density-dependent host selector that showed sharp selectivity at low density. X. ramesis and S. c. pyramidis were density-independent host selectors with a direct correspondence of density with habitat quality. N. i. theodori and S. t. medialis were non-selectors with no relationship at all between density and host quality. The results of the application of the isodar theory suggest that ectoparasites, like other animals, behave as if they are able to make choices and decisions that favour environments in which their reproductive benefit is maximized.     

Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance–occupancy relationship?

Relationships between hosts and parasites represent complex co-evolving systems that can vary both temporally and spatially. This variation may result in different phylogeographic outcomes, ranging from highly geographically structured parasite populations comprised of specialist lineages that are locally abundant but have restricted global occupancy to geographically unstructured parasite populations consisting of widespread parasites. Here, we present results from a large biogeographic study of the Leucocytozoon blood parasites of two nonmigrant bird species, conducted at nine sites across Europe. The aim was to determine whether the parasite lineages of the two hosts were phylogeographically structured across Europe. Employing molecular methods, we found a large diversity of parasites, and although overall prevalence varied greatly, the parasites were not genetically structured. Several measures of local parasite abundance were associated with the number of sites that the lineage occurred in, which is consistent with the macroecological phenomenon of the abundance-occupancy relationship. Taken together, our results show that parasite dispersal is somewhat uncoupled to that of the host in this system: we suggest that broad host and/or vector preference may play an important role in determining the distribution of these parasites and in affecting host-parasite coevolution in this system.     

Relative number of generations of hosts and parasites does not influence parasite local adaptation in coevolving populations of bacteria and phages

A potential consequence of host-parasite coevolution in spatially structured populations is parasite local adaptation: local parasites perform better than foreign parasites on their local host populations. It has been suggested that the generally shorter generation times of parasites compared with their hosts contributes to parasites, rather than hosts, being locally adapted. We tested the hypothesis that relative generation times of hosts and parasites affect local adaptation of hosts and parasites, using the bacterium Pseudomonas fluorescens and a lytic phage as host and parasite, respectively. Generation times were not directly manipulated, but instead one of the coevolving partners was regularly removed and replaced with a population from an earlier time point. Thus, one partner underwent more generations than the other. Manipulations were carried out at both early and later periods of coevolutionary interactions. At early stages of coevolution, host and parasites that underwent relatively more generations displayed higher levels of resistance and infectivity, respectively. However, the relative number of generations that bacteria and phages underwent did not change the level of local adaptation relative to control populations. This is likely because generalist hosts and parasites are favoured during early stages of coevolution, preventing local adaptation. By contrast, at later stages manipulations had no effect on either average levels of resistance or infectivity, or alter the level of local adaptation relative to the controls, possibly because traits other than resistance and infectivity were under strong selection. Taken together, these data suggest that the relative generation times of hosts and parasites may not be an important determinant of local adaptation in this system.     

Within-host competitive interactions as a mechanism for the maintenance of parasite diversity

Variation among parasite strains can affect the progression of disease or the effectiveness of treatment. What maintains parasite diversity? Here I argue that competition among parasites within the host is a major cause of variation among parasites. The competitive environment within the host can vary depending on the parasite genotypes present. For example, parasite strategies that target specific competitors, such as bacteriocins, are dependent on the presence and susceptibility of those competitors for success. Accordingly, which parasite traits are favoured by within-host selection can vary from host to host. Given the fluctuating fitness landscape across hosts, genotype by genotype (G×G) interactions among parasites should be prevalent. Moreover, selection should vary in a frequency-dependent manner, as attacking genotypes select for resistance and genotypes producing public goods select for cheaters. I review competitive coexistence theory with regard to parasites and highlight a few key examples where within-host competition promotes diversity. Finally, I discuss how within-host competition affects host health and our ability to successfully treat infectious diseases.     

Parasites promote host gene flow in a metapopulation

Local adaptation is a powerful mechanism to maintain genetic diversity in subdivided populations. It counteracts the homogenizing effect of gene flow because immigrants have an inferior fitness in the new habitat. This picture may be reversed in host populations where parasites influence the success of immigrating hosts. Here we report two experiments testing whether parasite abundance and genetic background influences the success of host migration among pools in a Daphnia magna metapopulation. In 22 natural populations of D. magna, immigrant hosts were found to be on average more successful when the resident populations experienced high prevalences of a local microsporidian parasite. We then determined whether this success is due to parasitism per se, or the genetic background of the parasites. In a common garden competition experiment, we found that parasites reduced the fitness of their local hosts relatively more than the fitness of allopatric host genotypes. Our experiments are consistent with theoretical predictions based on coevolutionary host-parasite models in metapopulations. A direct consequence of the observed mechanism is an elevated effective migration rate for the host in the metapopulation.     

Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata

Host-parasite coevolution is often described as a process of reciprocal adaptation and counter adaptation, driven by frequency-dependent selection. This requires that different parasite genotypes perform differently on different host genotypes. Such genotype-by-genotype interactions arise if adaptation to one host (or parasite) genotype reduces performance on others. These direct costs of adaptation can maintain genetic polymorphism and generate geographic patterns of local host or parasite adaptation. Fixation of all-resistant (or all-infective) genotypes is further prevented if adaptation trades off with other host (or parasite) life-history traits. For the host, such indirect costs of resistance refer to reduced fitness of resistant genotypes in the absence of parasites. We studied (co)evolution in experimental microcosms of several clones of the freshwater protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. After two and a half years of culture, inoculation of evolved and naive (never exposed to the parasite) hosts with evolved and founder parasites revealed an increase in host resistance, but not in parasite infectivity. A cross-infection experiment showed significant host clone-by-parasite isolate interactions, and evolved hosts tended to be more resistant to their own (local) parasites than to parasites from other hosts. Compared to naive clones, evolved host clones had lower division rates in the absence of the parasite. Thus, our study indicates de novo evolution of host resistance, associated with both direct and indirect costs. This illustrates how interactions with parasites can lead to the genetic divergence of initially identical populations.     

High-throughput analysis of growth differences among phage strains

Although methods such as spectrophotometry are useful for identifying growth differences among bacterial strains, it is currently difficult to similarly determine whether bacteriophage strains differ in growth using high throughput methods. Here we use automated spectrophotometry to develop an in vitro method for indirectly distinguishing fitness (growth) differences among virus strains, based on direct measures of their infected bacterial hosts. We used computer simulations of a mathematical model for phage growth to predict which features of bacterial growth curves were best associated with differences in growth among phage strains. We then tested these predictions using the in vitro method to confirm which of the inferred viral growth traits best reflected known fitness differences among genotypes of the RNA phage phi-6, when infecting a Pseudomonas syringae host. Results showed that the inferred phage trait of time-to-extinction (time required to drive bacterial density below detectable optical density) reliably correlated with genotype rankings based on absolute fitness (phage titer per ml). These data suggested that the high-throughput analysis was valuable for identifying growth differences among virus strains, and that the method may be especially useful for high throughput analyses of fitness differences among phage strains cultured and/or evolved in liquid (unstructured) environments.     

Parasitism, host immune defence and dispersal

Host-parasite interactions have been hypothesized to affect the evolution of dispersal by providing a possibility for hosts to escape debilitating parasites, and by influencing the level of local adaptation. We used a comparative approach to investigate the relationship between a component of host immune function (which reflects the evolutionary history of parasite-induced natural selection) and dispersal in birds. We used a sample of 46 species of birds for which we had obtained field estimates of T-cell response for nestlings, mainly from our own field studies in Denmark and Spain. Bird species with longer natal, but not with longer breeding dispersal distances had a stronger mean T-cell-mediated immune response in nestlings than species with short dispersal distances. That was also the case when controlling for the potentially confounding effect of migration from breeding to wintering area, which is known from previous studies to be positively associated with dispersal distance. These relationships held even when controlling for similarity among species because of common ancestry. Avian hosts with a larger number of different breeding habitats had weaker mean T-cell-mediated immune responses than habitat specialists. This relationship held even when controlling for similarity among species because of common ancestry. Therefore, T-cell-mediated immunity is an important predictor of evolutionary changes in dispersal ability among common European birds.     

The costs of evolving resistance in heterogeneous parasite environments

The evolution of host resistance to parasites, shaped by associated fitness costs, is crucial for epidemiology and maintenance of genetic diversity. Selection imposed by multiple parasites could be a particularly strong constraint, as hosts either accumulate costs of multiple specific resistances or evolve a more costly general resistance mechanism. We used experimental evolution to test how parasite heterogeneity influences the evolution of host resistance. We show that bacterial host populations evolved specific resistance to local bacteriophage parasites, regardless of whether they were in single or multiple-phage environments, and that hosts evolving with multiple phages were no more resistant to novel phages than those evolving with single phages. However, hosts from multiple-phage environments paid a higher cost, in terms of population growth in the absence of phage, for their evolved specific resistances than those from single-phage environments. Given that in nature host populations face selection pressures from multiple parasite strains and species, our results suggest that costs may be even more critical in shaping the evolution of resistance than previously thought. Furthermore, our results highlight that a better understanding of resistance costs under combined control strategies could lead to a more 'evolution-resistant' treatment of disease.     

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.     

HOST–PARASITE GENETIC INTERACTIONS AND VIRULENCE-TRANSMISSION RELATIONSHIPS IN NATURAL POPULATIONS OF MONARCH BUTTERFLIES

Evolutionary models predict that parasite virulence (parasite-induced host mortality) can evolve as a consequence of natural selection operating on between-host parasite transmission. Two major assumptions are that virulence and transmission are genetically related and that the relative virulence and transmission of parasite genotypes remain similar across host genotypes. We conducted a cross-infection experiment using monarch butterflies and their protozoan parasites from two populations in eastern and western North America. We tested each of 10 host family lines against each of 18 parasite genotypes and measured virulence (host life span) and parasite transmission potential (spore load). Consistent with virulence evolution theory, we found a positive relationship between virulence and transmission across parasite genotypes. However, the absolute values of virulence and transmission differed among host family lines, as did the rank order of parasite clones along the virulence-transmission relationship. Population-level analyses showed that parasites from western North America caused higher infection levels and virulence, but there was no evidence of local adaptation of parasites on sympatric hosts. Collectively, our results suggest that host genotypes can affect the strength and direction of selection on virulence in natural populations, and that predicting virulence evolution may require building genotype-specific interactions into simpler trade-off models.     

Antagonistic coevolution with parasites increases the cost of host deleterious mutations

The fitness consequences of deleterious mutations are sometimes greater when individuals are parasitized, hence parasites may result in the more rapid purging of deleterious mutations from host populations. The significance of host deleterious mutations when hosts and parasites antagonistically coevolve (reciprocal evolution of host resistance and parasite infectivity) has not previously been experimentally investigated. We addressed this by coevolving the bacterium Pseudomonas fluorescens and a parasitic bacteriophage in laboratory microcosms, using bacteria with high and low mutation loads. Directional coevolution between bacterial resistance and phage infectivity occurred in all populations. Bacterial population fitness, as measured by competition experiments with ancestral genotypes in the absence of phage, declined with time spent coevolving. However, this decline was significantly more rapid in bacteria with high mutation loads, suggesting the cost of bacterial resistance to phage was greater in the presence of deleterious mutations (synergistic epistasis). As such, resistance to phage was more costly to evolve in the presence of a high mutation load. Consistent with these data, bacteria with high mutation loads underwent less rapid directional coevolution with their phage populations, and showed lower levels of resistance to their coevolving phage populations. These data suggest that coevolution with parasites increases the rate at which deleterious mutations are purged from host populations.     

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 cost of phage resistance in a plant pathogenic bacterium is context‐dependent

Parasites are ubiquitous features of living systems and many parasites severely reduce the fecundity or longevity of their hosts. This parasite‐imposed selection on host populations should strongly favor the evolution of host resistance, but hosts typically face a trade‐off between investment in reproductive fitness and investment in defense against parasites. The magnitude of such a trade‐off is likely to be context‐dependent, and accordingly costs that are key in shaping evolution in nature may not be easily observable in an artificial environment. We set out to assess the costs of phage resistance for a plant pathogenic bacterium in its natural plant host versus in a nutrient‐rich, artificial medium. We demonstrate that mutants of Pseudomonas syringae that have evolved resistance via a single mutational step pay a substantial cost for this resistance when grown on their tomato plant hosts, but do not realize any measurable growth rate costs in nutrient‐rich media. This work demonstrates that resistance to phage can significantly alter bacterial growth within plant hosts, and therefore that phage‐mediated selection in nature is likely to be an important component of bacterial pathogenicity.     

Dispersal among habitats varying in fitness: reciprocating migration through ideal habitat selection

Current evolutionary models of dispersal set the ends of a continuum where the number of individuals emigrating from a habitat either equals the number of individuals immigrating (balanced dispersal) or where emigrants flow from a source habitat to a corresponding sink. Theories of habitat selection suggest a more sophisticated conditional strategy where individuals disperse from habitats where they have the greatest impact on fitness to habitats where their per capita impact is lower. Asymmetries between periods of population growth and decline result in a reciprocating dispersal strategy where the direction of migration is reversed as populations wax and wane. Thus, for example, if net migration of individuals flows from high- to low-density habitats during periods of population growth, net migration will flow in the opposite direction during population decline. Stochastic simulations and analytical models of reciprocating dispersal demonstrate that fitness, carrying capacity, stochastic dynamics, and interference from dominants interact to determine whether dispersal is balanced between habitats, or whether one habitat or the other acts as a net donor of dispersing individuals. While the pattern of dispersal may vary, each is consistent with an underlying strategy of density-dependent habitat selection.     

Trematode parasites infect or die in snail hosts

The Red Queen hypothesis is based on the assumption that parasites must genetically match their hosts to infect them successfully. If the parasites fail, they are assumed to be killed by the host's immune system. Here, we tested this using sympatric (mostly susceptible) and allopatric (mostly resistant) populations of a freshwater snail and its trematode parasite. We determined whether parasites which do not infect are either killed or passed through the host's digestive tract and remain infectious. Our results show that parasites do not get a second chance: they either infect or are killed by the host. The results suggest strong selection against parasites that are not adapted to local host genotypes.