Characteristics and drivers of plant virus community spatial patterns in US west coast grasslands

The spatial distribution of disease risk caused by multi‐pathogen infections is not frequently characterized, limiting understanding of the drivers of infection and thwarting prediction of future risk in a changing environment. Further complicating this predictive understanding is that interactions among multiple pathogens within a host commonly alter transmission success, infection risk, and disease dynamics. By characterizing spatial patterns of Barley and Cereal Yellow Dwarf Virus (B/CYDV) infections that range from the scale of an individual plant to thousands of neighboring plants, we examined the contributions of spatial processes to the distribution of disease risk. In a two‐year field experiment, we planted grass hosts of B/CYDVs into fertilized plots of US west coast grasslands. We determined how vector‐sharing, environmental conditions and spatial variation in host quality affected spatial patterns of single viruses, pairs of viruses and the whole virus community across out‐planted grass hosts. We found that single viruses and virus communities were spatially random, indicating that infection does not solely spread through the community in a wave‐like manner. On the other hand, we found that pairs of viruses, especially those that share a vector species, were aggregated spatially. This suggests that if within‐host competition exists, it is not strong. Aggregation in one pair of viruses was more frequent due to environmental conditions and spatial variation in out‐planted host quality, measured as vector preference. These results highlight the importance of insect vectors for predicting the spatial distribution of coinfection risk by B/CYDVs.     

Vector within‐host feeding preference mediates transmission of a heterogeneously distributed pathogen

1. Ecological theory predicts that vector preference for certain host species or discrimination between infected versus uninfected hosts impacts disease incidence. However, little information exists on the extent to which vector within‐host feeding preference mediates transmission. This may be particularly important for plant pathogens, such as sharpshooter transmission of the bacterium Xylella fastidiosa, which are distributed irregularly throughout hosts. 2. We documented the within‐host distribution of two vector species that differ in transmission efficiency, the leafhoppers Draeculacephala minerva and Graphocephala atropunctata, and which are free to move throughout entirely caged alfalfa plants. The more efficient vector D. minerva fed preferentially at the base of the plant near the soil surface, whereas the less efficient G. atropunctata preferred overwhelming the top of the plant. 3. Next we documented X. fastidiosa heterogeneity in mechanically inoculated plants. Infection rates were up to 50% higher and mean bacterial population densities were 100‐fold higher near the plant base than at the top or in the taproot. 4. Finally, we estimated transmission efficiency of the two leafhoppers when they were confined at either the base or top of inoculated alfalfa plants. Both vectors were inefficient when confined at the top of infected plants and were 20–60% more efficient when confined at the plant base. 5. These results show that vector transmission efficiency is determined by the interaction between leafhopper within‐plant feeding behaviour and pathogen within‐plant distribution. Fine‐scale vector and pathogen overlap is likely to be a requirement generally for efficient transmission of vector‐borne pathogens.     

Parasite consumption and host interference can inhibit disease spread in dense populations

Disease dynamics hinge on parasite transmission among hosts. However, canonical models for transmission often fit data poorly, limiting predictive ability. One solution involves building mechanistic yet general links between host behaviour and disease spread. To illustrate, we focus on the exposure component of transmission for hosts that consume their parasites, combining experiments, models and field data. Models of transmission that incorporate parasite consumption and foraging interference among hosts vastly outperformed alternatives when fit to experimental data using a zooplankton host (Daphnia dentifera) that consumes spores of a fungus (Metschnikowia bicuspidata). Once plugged into a fully dynamic model, both mechanisms inhibited epidemics overall. Foraging interference further depressed parasite invasion and prevalence at high host density, creating unimodal (hump‐shaped) relationships between host density and these indices. These novel results qualitatively matched a unimodal density–prevalence relationship in natural epidemics. Ultimately, a mechanistic approach to transmission can reveal new insights into disease outbreaks.     

Ticks need not bite their red grouse hosts to infect them with louping ill virus

For pathogens transmitted by biting vectors, one of the fundamental assumptions is often that vector bites are the sole or main route of host infection. Here, we demonstrate experimentally a transmission route whereby hosts (red grouse, Lagopus lagopus scoticus) became infected with a member of the tick-borne encephalitis virus complex, louping ill virus, after eating the infected tick vector. Furthermore, we estimated from field observations that this mode of infection could account for 73-98% of all virus infections in wild red grouse in their first season. This has potential implications for the understanding of other biting vector-borne pathogens where hosts may ingest vectors through foraging or grooming.     

The evolution of virulence in pathogens with frequency-dependent transmission

Frequency-dependent transmission is an important feature of diseases that are sexually transmitted or transmitted by a vector that actively searches for hosts. Here I describe the evolution of virulence in pathogens that have frequency-dependent transmission. I consider two components of virulence--an increase in host mortality due to infection, as is classically described, and a decrease in host fecundity due to infection, because frequency dependence is common among diseases that fully or partially sterilize their hosts. Theoretical predictions pertaining to host-pathogen numerical dynamics can be quite different between pathogens with frequency-dependent transmission and those with density-dependent transmission. In contrast, this study suggests that the principles governing the evolution of virulence that have been established in the context of density-dependent pathogens may also apply (qualitatively) to frequency-dependent pathogens. I examine the evolutionary trajectories of the mortality and sterility components of virulence as well as the role of spatial population structure in the evolution of the sterility component of virulence.     

Spatiotemporal Model of Barley and Cereal Yellow Dwarf Virus Transmission Dynamics with Seasonality and Plant Competition

Many generalist pathogens are influenced by the spatial distributions and relative abundances of susceptible host species. The spatial structure of host populations can influence patterns of infection incidence (or disease outbreaks), and the effects of a generalist pathogen on host community dynamics in a spatially heterogeneous community may differ from predictions derived via simple models. In this paper, we model the transmission of a generalist pathogen within a patch framework that incorporates the movement of vectors between discrete host patches to investigate the effects of local host community composition and vector movement rates on disease dynamics.     

Phylogenetic evidence of host-specific cryptic species in the anther smut fungus

Cryptic structure of species complexes confounds an accurate accounting of biological diversity in natural systems. Also, cryptic sibling species often become specialized to different ecological conditions, for instance, with host specialization by cryptic parasite species. The fungus Microbotryum violaceum causes anther smut disease in plants of Caryophyllaceae, and the degree of specialization and gene flow between strains on different hosts have been controversial in the literature. We conducted molecular phylogenetic analyses on M. violaceum from 23 host species and different geographic origins using three single-copy nuclear genes (beta-tub, gamma-tub, and Ef1alpha). Congruence between the phylogenies identified several lineages that evolved independently for a long time. The lineages had overlapping geographic ranges but were highly specialized on different hosts. These results thus suggest that M. violaceum is a complex of highly specialized sibling species. Two incongruencies between the individual gene phylogenies and one intragene recombination event were detected at basal nodes, suggesting ancient introgression events or speciation events via hybridizations. However, incongruencies and recombination were not detected among terminal branches, indicating that the potentials for cross-infection and experimental hybridization are often not sufficient to suggest that introgressions would likely persist in nature.     

Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission

The influence of host diversity on multi-host pathogen transmission and persistence can be confounded by the large number of species and biological interactions that can characterize many transmission systems. For vector-borne pathogens, the composition of host communities has been hypothesized to affect transmission; however, the specific characteristics of host communities that affect transmission remain largely unknown. We tested the hypothesis that vector host use and force of infection (i.e., the summed number of infectious mosquitoes resulting from feeding upon each vertebrate host within a community of hosts), and not simply host diversity or richness, determine local infection rates of West Nile virus (WNV) in mosquito vectors. In suburban Chicago, Illinois, USA, we estimated community force of infection for West Nile virus using data on Culex pipiens mosquito host selection and WNV vertebrate reservoir competence for each host species in multiple residential and semi-natural study sites. We found host community force of infection interacted with avian diversity to influence WNV infection in Culex mosquitoes across the study area. Two avian species, the American robin (Turdus migratorius) and the house sparrow (Passer domesticus), produced 95.8% of the infectious Cx. pipiens mosquitoes and showed a significant positive association with WNV infection in Culex spp. mosquitoes. Therefore, indices of community structure, such as species diversity or richness, may not be reliable indicators of transmission risk at fine spatial scales in vector-borne disease systems. Rather, robust assessment of local transmission risk should incorporate heterogeneity in vector host feeding and variation in vertebrate reservoir competence at the spatial scale of vector-host interaction.     

Intraspecific variation in herbivore‐induced plant volatiles influences the spatial range of plant–parasitoid interactions

Chemical information influences the behaviour of many animals, thus affecting species interactions. Many animals forage for resources that are heterogeneously distributed in space and time, and have evolved foraging behaviour that utilizes information related to these resources. Herbivore‐induced plant volatiles (HIPVs), emitted by plants upon herbivore attack, provide information on herbivory to various animal species, including parasitoids. Little is known about the spatial scale at which plants attract parasitoids via HIPVs under field conditions and how intraspecific variation in HIPV emission affects this spatial scale. Here, we investigated the spatial scale of parasitoid attraction to two cabbage accessions that differ in relative preference of the parasitoid Cotesia glomerata when plants were damaged by Pieris brassicae caterpillars. Parasitoids were released in a field experiment with plants at distances of up to 60 m from the release site using intervals between plants of 10 or 20 m to assess parasitism rates over time and distance. Additionally, we observed host‐location behaviour of parasitoids in detail in a semi‐field tent experiment with plant spacing up to 8 m. Plant accession strongly affected successful host location in field set‐ups with 10 or 20 m intervals between plants. In the semi‐field set‐up, plant finding success by parasitoids decreased with increasing plant spacing, differed between plant accessions, and was higher for host‐infested plants than for uninfested plants. We demonstrate that parasitoids can be attracted to herbivore‐infested plants over large distances (10 m or 20 m) in the field, and that stronger plant attractiveness via HIPVs increases this distance (up to at least 20 m). Our study indicates that variation in plant traits can affect attraction distance, movement patterns of parasitoids, and ultimately spatial patterns of plant–insect interactions. It is therefore important to consider plant‐trait variation in HIPVs when studying animal foraging behaviour and multi‐trophic interactions in a spatial context.     

Local adaptation in the Linum marginale-Melampsora lini host-pathogen interaction

The potential for local adaptation between pathogens and their hosts has generated strong theoretical and empirical interest with evidence both for and against local adaptation reported for a range of systems. We use the Linum marginale-Melampsora lini plant-pathogen system and a hierarchical spatial structure to investigate patterns of local adaptation within a metapopulation characterised by epidemic dynamics and frequent extinction of pathogen populations. Based on large sample sizes and comprehensive cross-inoculation trials, our analyses demonstrate strong local adaptation by Melampsora to its host populations, with this effect being greatest at regional scales, as predicted from the broader spatial scales at which M. lini disperses relative to L. marginale. However, there was no consistent trend for more distant pathogen populations to perform more poorly. Our results further show how the coevolutionary interaction between hosts and pathogens can be influenced by local structure such that resistant hosts select for generally virulent pathogens, while susceptible hosts select for more avirulent pathogens. Empirically, local adaptation has generally been tested in two contrasting ways: (1) pathogen performance on sympatric versus allopatric hosts; and (2) sympatric versus allopatric pathogens on a given host population. In situations where no host population is more resistant or susceptible than others when averaged across pathogen populations (and likewise, no pathogen population is more virulent or avirulent than others), results from these tests should generally be congruent. We argue that this is unlikely to be the case in the metapopulation situations that predominate in natural host-pathogen interactions, thus requiring tests that control simultaneously for variation in plant and pathogen populations.     

The influence of host demography, pathogen virulence, and relationships with pathogen virulence on the evolution of pathogen transmission in a spatial context

A major challenge in evolutionary ecology is to explain extensive natural variation in transmission rates and virulence across pathogens. Host and pathogen ecology is a potentially important source of that variation. Theory of its effects has been developed through the study of non-spatial models, but host population spatial structure has been shown to influence evolutionary outcomes. To date, the effects of basic host and pathogen demography on pathogen evolution have not been thoroughly explored in a spatial context. Here we use simulations to show that space produces novel predictions of the influence of the shape of the pathogen’s transmission–virulence tradeoff, as well as host reproduction and mortality, on the pathogen’s evolutionary stable transmission rate. Importantly, non-spatial models predict that neither the slope of linear transmission–virulence relationships, nor the host reproduction rate will influence pathogen evolution, and that host mortality will only influence it when there is a transmission–virulence tradeoff. We show that this is not the case in a spatial context, and identify the ecological conditions under which spatial effects are most influential. Thus, these results may help explain observed natural variation among pathogens unexplainable by non-spatial models, and provide guidance about when space should be considered. We additionally evaluate the ability of existing analytical approaches to predict the influence of ecology, namely spatial moment equations closed with an improved pair approximation (IPA). The IPA is known to have limited accuracy, but here we show that in the context of pathogens the limitations are substantial: in many cases, IPA incorrectly predicts evolution to pathogen-driven extinction. Despite these limitations, we suggest that the impact of ecology can still be understood within the conceptual framework arising from spatial moment equations, that of “self-shading’’, whereby the spread of highly transmissible pathogens is impeded by local depletion of susceptible hosts.     

HOST POPULATION STRUCTURE AND THE EVOLUTION OF VIRULENCE: A “LAW OF DIMINISHING RETURNS”

Structure in a population of host individuals, whether spatial or temporal, can have important effects on the transmission and evolutionary dynamics of its pathogens. One of these is to limit dispersal of pathogens and thus increase the amount of contact between a given pair or within a small group of host individuals. We introduce a “law of diminishing returns” that predicts an evolutionary decline of pathogen virulence whenever there are on average more possibilities of pathogen transmission between the same pair of hosts. Thus, the effect of repeated contact between hosts will be to shift the balance of any trade-off between virulence and transmissibility toward lower virulence.     

Vector-Borne Pathogen and Host Evolution in a Structured Immuno-Epidemiological System

Vector-borne disease transmission is a common dissemination mode used by many pathogens to spread in a host population. Similar to directly transmitted diseases, the within-host interaction of a vector-borne pathogen and a host’s immune system influences the pathogen’s transmission potential between hosts via vectors. Yet there are few theoretical studies on virulence–transmission trade-offs and evolution in vector-borne pathogen–host systems. Here, we consider an immuno-epidemiological model that links the within-host dynamics to between-host circulation of a vector-borne disease. On the immunological scale, the model mimics antibody-pathogen dynamics for arbovirus diseases, such as Rift Valley fever and West Nile virus. The within-host dynamics govern transmission and host mortality and recovery in an age-since-infection structured host-vector-borne pathogen epidemic model. By considering multiple pathogen strains and multiple competing host populations differing in their within-host replication rate and immune response parameters, respectively, we derive evolutionary optimization principles for both pathogen and host. Invasion analysis shows that the \({\mathcal {R}}_0\) maximization principle holds for the vector-borne pathogen. For the host, we prove that evolution favors minimizing case fatality ratio (CFR). These results are utilized to compute host and pathogen evolutionary trajectories and to determine how model parameters affect evolution outcomes. We find that increasing the vector inoculum size increases the pathogen \({\mathcal {R}}_0\), but can either increase or decrease the pathogen virulence (the host CFR), suggesting that vector inoculum size can contribute to virulence of vector-borne diseases in distinct ways.     

Pathogens manipulate the preference of vectors,slowing disease spread in a multi‐host system

The spread of vector‐borne pathogens depends on a complex set of interactions among pathogen, vector, and host. In single‐host systems, pathogens can induce changes in vector preferences for infected vs. healthy hosts. Yet it is unclear if pathogens also induce changes in vector preference among host species, and how changes in vector behaviour alter the ecological dynamics of disease spread. Here, we couple multi‐host preference experiments with a novel model of vector preference general to both single and multi‐host communities. We show that viruliferous aphids exhibit strong preferences for healthy and long‐lived hosts. Coupling experimental results with modelling to account for preference leads to a strong decrease in overall pathogen spread through multi‐host communities due to non‐random sorting of viruliferous vectors between preferred and non‐preferred host species. Our results demonstrate the importance of the interplay between vector behaviour and host diversity as a key mechanism in the spread of vectored‐diseases.     

Avian malaria infection intensity influences mosquito feeding patterns

Pathogen-induced host phenotypic changes are widespread phenomena that can dramatically influence host–vector interactions. Enhanced vector attraction to infected hosts has been reported in a variety of host–pathogen systems, and has given rise to the parasite manipulation hypothesis whereby pathogens may adaptively modify host phenotypes to increase transmission from host to host. However, host phenotypic changes do not always favour the transmission of pathogens, as random host choice, reduced host attractiveness and even host avoidance after infection have also been reported. Thus, the effects of hosts’ parasitic infections on vector feeding behaviour and on the likelihood of parasite transmission remain unclear. Here, we experimentally tested how host infection status and infection intensity with avian Plasmodium affect mosquito feeding patterns in house sparrows (Passer domesticus). In separate experiments, mosquitoes were allowed to bite pairs containing (i) one infected and one uninfected bird and (ii) two infected birds, one of which treated with the antimalarial drug, primaquine. We found that mosquitoes fed randomly when exposed to both infected and uninfected birds. However, when mosquitoes were exposed only to infected individuals, they preferred to bite the non-treated birds. These results suggest that the malarial parasite load rather than the infection itself plays a key role in mosquito attraction. Our findings partially support the parasite manipulation hypothesis, which probably operates via a reduction in defensive behaviour, and highlights the importance of considering parasite load in studies on host–vector–pathogen interactions.     

Host spatial heterogeneity and the spread of vector-borne infection.

We analyze how spatial heterogeneity in host density affects the advance of vector-borne disease. Infection requires vector infestation. The vector spreads only between hosts occupying the same neighborhood, and the number of hosts varies randomly among neighborhoods. Simulation of a spatially detailed model shows that increasing heterogeneity in host abundance reduces pathogen prevalence. Clumping of hosts can limit the advance of the vector, which inhibits the spread of infection indirectly. Clumping can also increase the chance that the pathogen and vector become physically separated during the initial phase of the epidemic process. The latter limitation on the pathogen's spread, in our simulations, is restricted to small interaction neighborhoods. A mean-field model, which does not maintain spatial correlations between sites, approximates simulation results when hosts are arrayed uniformly, but overestimates infection prevalence when hosts are aggregated. A pair approximation, which includes some of the simulation model's spatial correlations, better describes the vector infestation frequencies across host spatial dispersions.     

Influence of host distribution on foraging behaviour in the hyperparasitoid wasp, Dendrocerus carpenteri

The foraging behaviour of Dendrocerus carpenteriCurtis (Hymenoptera: Megaspilidae), an ectophagous hyperparasitoid of aphidiine wasps inside mummified aphids, was examined in the laboratory with an experimental system consisting of broad bean, Vicia fabaL, the pea aphid, Acyrthosiphon pisumHarris, and a primary parasitoid, Ephedrus californicusBaker. Pea aphids parasitised by E. californicusoften disperse from their feeding sites (or off host plants) before dying and mummifying. Response of female hyperparasitoids to host distribution was evaluated at two spatial scales. At the first scale, behaviour of hyperparasitoids was examined on individual plants with different densities of hosts. At the second scale, habitat complexity and host location were manipulated in large foraging cages containing several plants. I show that patterns of density-dependent hyperparasitism can result from the foraging behaviour of D. carpenteri. However, dispersal of parasitised aphids may not reduce the incidence of hyperparasitism if hyperparasitoids systematically search the habitat.     

The spatial distribution of plant populations, disease dynamics and evolution of resistance

Empirical studies of the interaction between the anther smut fungus Microbotryum violaceum and its host plant Lychnis alpina were combined with modelling approaches to investigate how variation in the spatial distribution of host populations influences disease dynamics and variation in resistance. Patterns of disease incidence and prevalence were surveyed in three contrasting systems of natural L . alpina populations where there is substantial variation in spatial structure, ranging from large continuous populations through to small isolated patches. Disease incidence (fraction of populations where disease was present) was highest in the continuous situation, and lowest in the most isolated populations. The reverse was true for prevalence (fraction of individuals diseased). To better understand the long-term ecological and evolutionary consequences of differences in among population spatial structure, we developed a two-dimensional spatially explicit simulation model in which host-population spacing was modelled by varying the percentage of sites suitable for the host. The general patterns of disease incidence and prevalence generated in the simulations corresponded well with the patterns observed in natural populations of L. alpina and M. violaceum ; i.e. the fraction of sites with disease increased while the average disease prevalence in diseased populations decreased when host populations became more connected. One likely explanation for the differences in disease incidence and prevalence seen in natural populations is that the evolution of host resistance varies as a function of the degree of fragmentation. This is supported by simulation results that were qualitatively similar to the survey data when resistance was allowed to vary, but not when hosts were assumed to be uniformly susceptible. In the former, the frequency of resistance increased markedly as host populations became more connected.     

Patterns of virulence and benevolence in insect‐borne pathogens of plants

Direct and indirect interactions between insect‐borne pathogens and their host plants are reviewed in the context of theoretical analyses of the evolution of virulence. Unlike earlier theories, which maintained that parasites should evolve to be harmless or even beneficial to their hosts, recent models predict that coevolution between pathogen and host may lead to virulence or avirulence, depending on the pathogen transmission system. The studies reviewed here support the hypothesis that virulence can be advantageous for insect‐borne pathogens of plants. Virulent pathogens may be transmitted more readily by vector insects and are likely to induce stronger disease symptoms, thereby potentially making the plant more attractive to vectors. In contrast, the transmission advantage of virulence for seed‐transmitted pathogens is lower and the costs of virulence are high. Pathogens may sometimes benefit plants via indirect interactions that arise through relationships with other organisms. Evidence for the effects of insect‐borne pathogens on plant competition, herbivory, and parasitism also is reviewed, but few studies have measured the outcome of both direct and indirect interactions. Benefits of pathogen infection that accrue to plants from indirect interactions may sometimes outweigh the direct detrimental effects of virulence.     

Density-dependent foraging behaviors in a parasitoid lead to density-dependent parasitism of its host

Empirical studies of spatial heterogeneity in parasitism by insect parasitoids have focused largely on patterns, while the many possible underlying mechanisms have been little studied in the field. We conducted experimental and observational studies on Tachinomyia similis (Diptera: Tachinidae) attacking western tussock moths (Orgyia vetusta; Lepidoptera: Lymantriidae) on lupine bushes at Bodega Bay, Calif., USA. We examined several foraging behaviors that have been hypothesized to create density-dependent variation in parasitism rates, including spatial aggregation of parasitoids to high host density, mutual interference among searching parasitoids and decelerating functional responses of the parasitoid. At the spatial scale of individual bushes, we detected both aggregation to a high density and a decelerating functional response. The resulting spatial pattern of parasitism was best fit by two models; one included an effect of parasitoid aggregation and the other included an effect of aggregation and a decelerating functional response. Most of the variation in parasitism was not correlated with density of O. vetusta.