Richness and Composition of Niche-Assembled Viral Pathogen Communities

The pathogen and parasite community that inhabits every free-living organism can control host vital rates including lifespan and reproductive output. To date, however, there have been few experiments examining pathogen community assembly replicated at large-enough spatial scales to inform our understanding of pathogen dynamics in natural systems. Pathogen community assembly may be driven by neutral stochastic colonization and extinction events or by niche differentiation that constrains pathogen distributions to particular environmental conditions, hosts, or vectors.Here, we present results from a regionally-replicated experiment investigating the community of barley and cereal yellow dwarf viruses (B/CYDV''s) in over 5000 experimentally planted individuals of six grass species along a 700 km latitudinal gradient along the Pacific coast of North America (USA) in response to experimentally manipulated nitrogen and phosphorus supplies. The composition of the virus community varied predictably among hosts and across nutrient-addition treatments, indicating niche differentiation among virus species. There were some concordant responses among the viral species. For example, the prevalence of most viral species increased consistently with perennial grass cover, leading to a 60% increase in the richness of the viral community within individual hosts (i.e., coinfection) in perennial-dominated plots. Furthermore, infection rates of the six host species in the field were highly correlated with vector preferences assessed in laboratory trials. Our results reveal the importance of niche differentiation in structuring virus assemblages. Virus species distributions reflected a combination of local host community composition, host species-specific vector preferences, and virus responses to host nutrition. In addition, our results suggest that heterogeneity among host species in their capacity to attract vectors or support pathogens between growing seasons can lead to positive covariation among virus species.     

Mixed infection,risk projection,and misdirection: Interactions among pathogens alter links between host resources and disease

A growing body of literature links resources of hosts to their risk of infectious disease. Yet most hosts encounter multiple pathogens, and projections of disease risk based on resource availability could be fundamentally wrong if they do not account for interactions among pathogens within hosts. Here, we measured infection risk of grass hosts (Avena sativa) exposed to three naturally co‐occurring viruses either singly or jointly (barley and cereal yellow dwarf viruses [B/CYDVs]: CYDV‐RPV, BYDV‐PAV, and BYDV‐SGV) along experimental gradients of nitrogen and phosphorus supply. We asked whether disease risk (i.e., infection prevalence) differed in single versus co‐inoculations, and whether these differences varied with rates and ratios of nitrogen and phosphorus supply. In single inoculations, the viruses did not respond strongly to nitrogen or phosphorus. However, in co‐inoculations, we detected illustrative cases of 1) resource‐dependent antagonism (lower prevalence of RPV with increasing N; possibly due to competition), 2) resource‐dependent facilitation (higher prevalence of SGV with decreasing N:P; possibly due to immunosuppression), and 3) weak or no interactions within hosts (for PAV). Together, these within‐host interactions created emergent patterns for co‐inoculated hosts, with both infection prevalence and viral richness increasing with the combination of low nitrogen and high phosphorus supply. We demonstrate that knowledge of multiple pathogens is essential for predicting disease risk from host resources and that projections of risk that fail to acknowledge resource‐dependent interactions within hosts could be qualitatively wrong. Expansions of theory from community ecology theory may help anticipate such relationships by linking host resources to diverse pathogen communities.     

Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses

In California valley grasslands, Avena fatua L. and other exotic annual grasses have largely displaced native perennial bunchgrasses such as Elymus glaucus Buckley and Nassella pulchra (A. Hitchc.) Barkworth. The invasion success and continued dominance of the exotics has been generally attributed to changes in disturbance regimes and the outcome of direct competition between species. Here, we report that exotic grasses can also indirectly increase disease incidence in nearby native grasses. We found that the presence of A. fatua more than doubled incidence of infection by barley and cereal yellow dwarf viruses (B/CYDVs) in E. glaucus. Because B/CYDV infection can stunt E. glaucus and other native bunchgrasses, the indirect effects of A. fatua on virus incidence in natives suggests that apparent competition may be an additional mechanism influencing interactions among exotic and native grasses in California. A. fatua's influence on virus incidence is likely mediated by its effects on populations of aphids that vector B/CYDVs. In our study, aphids consistently preferred exotic annuals as hosts and experienced higher fecundity on them, suggesting that the exotics can attract and amplify vector populations. To the best of our knowledge, these findings are the first demonstration that exotic plants can indirectly influence virus incidence in natives. We suggest that invasion success may be influenced by the capacity of exotic plant species to increase the pathogen loads of native species with which they compete.     

Ecological dynamics of emerging bat virus spillover

Viruses that originate in bats may be the most notorious emerging zoonoses that spill over from wildlife into domestic animals and humans. Understanding how these infections filter through ecological systems to cause disease in humans is of profound importance to public health. Transmission of viruses from bats to humans requires a hierarchy of enabling conditions that connect the distribution of reservoir hosts, viral infection within these hosts, and exposure and susceptibility of recipient hosts. For many emerging bat viruses, spillover also requires viral shedding from bats, and survival of the virus in the environment. Focusing on Hendra virus, but also addressing Nipah virus, Ebola virus, Marburg virus and coronaviruses, we delineate this cross-species spillover dynamic from the within-host processes that drive virus excretion to land-use changes that increase interaction among species. We describe how land-use changes may affect co-occurrence and contact between bats and recipient hosts. Two hypotheses may explain temporal and spatial pulses of virus shedding in bat populations: episodic shedding from persistently infected bats or transient epidemics that occur as virus is transmitted among bat populations. Management of livestock also may affect the probability of exposure and disease. Interventions to decrease the probability of virus spillover can be implemented at multiple levels from targeting the reservoir host to managing recipient host exposure and susceptibility.     

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.     

Spatial determinants of infection risk in a multi‐species avian malaria system

Spatially‐variable processes can be an important element of host–parasite interactions, but their longer term demographic and evolutionary effects depend on the magnitude of variation in space, the scale at which variation occurs and the degree to which such processes are temporally stable. Here, we use multiple years of data from a study of two closely related tit species (Paridae), infected with two congeneric species of avian malaria (Plasmodium), to evaluate the roles of extrinsic and intrinsic factors in driving spatial heterogeneity in infection risk, and to address questions of scale and temporal stability in these vector‐driven host–parasite interactions. We show that the two malaria parasite species exhibit markedly different spatial epidemiology: P. relictum infections are effectively randomly distributed in space, with no temporal consistency, whereas P. circumflexum infections exhibit pronounced spatial structuring that is stable over the six years of this study and similar in both host species. We show that both conspecific and heterospecific host density contribute to elevated infection risk, but that the main determinants of elevated risk of P. circumflexum infection risk are habitat features probably associated with vector distribution and abundance. We discuss the implications of these findings, both for our understanding of the epidemiology of malaria in the wild, but also in terms of the longer‐term evolutionary and demographic consequences that spatially variable parasite‐mediated selection may have on host populations.     

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.     

A continental risk assessment of West Nile virus under climate change

Since first introduced to North America in 1999, West Nile virus (WNV) has spread rapidly across the continent, threatening wildlife populations and posing serious health risks to humans. While WNV incidence has been linked to environmental factors, particularly temperature and rainfall, little is known about how future climate change may affect the spread of the disease. Using available data on WNV infections in vectors and hosts collected from 2003–2011 and using a suite of 10 species distribution models, weighted according to their predictive performance, we modeled the incidence of WNV under current climate conditions at a continental scale. Models were found to accurately predict spatial patterns of WNV that were then used to examine how future climate may affect the spread of the disease. Predictions were accurate for cases of human WNV infection in the following year (2012), with areas reporting infections having significantly higher probability of presence as predicted by our models. Projected geographic distributions of WNV in North America under future climate for 2050 and 2080 show an expansion of suitable climate for the disease, driven by warmer temperatures and lower annual precipitation that will result in the exposure of new and naïve host populations to the virus with potentially serious consequences. Our risk assessment identifies current and future hotspots of West Nile virus where mitigation efforts should be focused and presents an important new approach for monitoring vector‐borne disease under climate change.     

Knock‐on community impacts of a novel vector: spillover of emerging DWV‐B from Varroa‐infested honeybees to wild bumblebees

Novel transmission routes can directly impact the evolutionary ecology of infectious diseases, with potentially dramatic effect on host populations and knock‐on effects on the wider host community. The invasion of Varroa destructor, an ectoparasitic viral vector in Western honeybees, provides a unique opportunity to examine how a novel vector affects disease epidemiology in a host community. This specialist honeybee mite vectors deformed wing virus (DWV), an important re‐emerging honeybee pathogen that also infects wild bumblebees. Comparing island honeybee and wild bumblebee populations with and without V. destructor, we show that V. destructor drives DWV prevalence and titre in honeybees and sympatric bumblebees. Viral genotypes are shared across hosts, with the potentially more virulent DWV‐B overtaking DWV‐A in prevalence in a current epidemic. This demonstrates disease emergence across a host community driven by the acquisition of a specialist novel transmission route in one host, with dramatic community level knock‐on effects.     

Spatiotemporal patterns of avian host–parasite interactions in the face of biogeographical range expansions

Exploration of interactions between hosts and parasitic symbionts is important for our understanding of the temporal and spatial distribution of organisms. For example, host colonization of new geographical regions may alter levels of infections and parasite specificity, and even allow hosts to escape from co‐evolved parasites, consequently shaping spatial distributions and community structure of both host and parasite. Here we investigate the effect of host colonization of new regions and the elevational distribution of host–parasite associations between birds and their vector‐transmitted haemosporidian blood parasites in two geological and geographical settings: mountains of New Guinea and the Canary Islands. Our results demonstrate that bird communities in younger regions have significantly lower levels of parasitism compared to those of older regions. Furthermore, host–parasite network analyses demonstrate that blood parasites may respond differently after arriving to a new region, through adaptations that allow for either expanding (Canary Islands) or retaining (New Guinea) their host niches. The spatial prevalence patterns along elevational gradients differed in the two regions, suggesting that region‐specific biotic (e.g., host community) and abiotic factors (e.g., temperature) govern prevalence patterns. Our findings suggest that the spatiotemporal range dynamics in host–parasite systems are driven by multiple factors, but that host and parasite community compositions and colonization histories are of particular importance.     

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.     

The importance of environmental spatial heterogeneity and host social structure in disease transmission

[First paragraph]The spatial structure of a host population determines the spatial probability distribution of interaction between individuals, and therefore influences the spatio-temporal dynamics of disease transmission within the host population (Keeling, 1999; Gudelj and White, 2004). Nigel Barlow recognised this and included non-linear transmission in his later models (Barlow, 1991), simulating the result of spatial heterogeneity of risk in susceptible hosts. These models produced behaviour that could not be found in models with homogeneously mixed host populations: more rapid disease dynamics and a greater robustness of disease to control measures. However, in this model there was no causal mechanism driving the initial spatial heterogeneity of risk in host individuals. Environmental heterogeneity is likely to be a key factor in determining the spatial distribution of host individuals (Cronin and Reeve, 2005). We attempted to explore how environmental heterogeneity may affect disease dynamics via its influence on the spatial distribution of host individuals. We developed a spatially explicit stochastic model that incorporated spatially variable host density distributions, primarily driven by environmental heterogeneity.     

The effect of landscape heterogeneity and host movement on a tick-borne pathogen

Landscape heterogeneity can be instrumental in determining local disease risk, pathogen persistence and spread. This is because different landscape features such as habitat type determine the abundance and spatial distributions of hosts and pathogen vectors. Therefore, disease prevalence and distribution are intrinsically linked to the hosts and vectors that utilise the different habitats. Here, we develop a simplified reaction diffusion model of the louping-ill virus and red grouse (Lagopus lagopus scoticus) system to investigate the occurrence of a tick-borne pathogen and the effect of host movement and landscape structure. Ticks (Ixodes ricinus), the virus-vector, are dispersed by a virally incompetent tick host, red deer (Cervus elephus), between different habitats, whilst the virus infects only red grouse. We investigated how deer movement between different habitats (forest and moorland) affected tick distribution and hence prevalence of infected ticks and grouse and hence, the effect of habitat size ratio and fragmentation on infection. When habitat type has a role in the survival of the pathogen vector, we demonstrated that habitat fragmentation can have a considerable effect on infection. These results highlight the importance of landscape heterogeneity and the proximity and size of adjacent habitats when predicting disease risk in a particular location. In addition, this model could be useful for other pathogen systems with generalist vectors and may inform policy on possible disease management strategies that incorporate host movements.     

Host physiological phenotype explains pathogen reservoir potential

Control of emerging infectious diseases often hinges on identifying a pathogen reservoir, the source of disease transmission. The potential to function as a pathogen reservoir can be influenced by host lifespan, geographic provenance and phylogeny. Yet, no study has identified factors that causally determine the reservoir potential of diverse host species. We propose the host physiological phenotype hypothesis, which predicts that hosts with short‐lived, poorly defended, nutrient rich and high metabolism tissue have greater values for three epidemiological parameters that determine reservoir potential: host susceptibility to infection, competence to infect vectors and ability to support vector populations. We experimentally tested these predictions using a generalist vectored virus and six wild grass species. Host physiological phenotype explained why hosts differed in all three epidemiological parameters while host lifespan, provenance and phylogeny could not explain host competence. Thus, a single, general axis describing variation in host physiological phenotype may explain reservoir potential.     

Effects of mammal host diversity and density on the infection level of Trypanosoma cruzi in sylvatic kissing bugs

Several reports have described host species diversity and identity as the most important factors influencing disease risk, producing either dilution or amplification of the pathogen in a host community. Triatomine vectors, mammals and the protozoan Trypanosoma cruzi (Trypanosomatida: Trypanosomatidae) Chagas are involved in the wild cycle of Chagas disease, in which infection of mammals occurs by contamination of mucous membranes or skin abrasions with insect‐infected faeces. We examined the extent to which host diversity and identity determine the infection level observed in vector populations (i.e. disease risk in humans). We recorded infection in triatomine colonies and on the coexisting host mammalian species in semi‐arid Chile. Host diversity, and total and infected host species densities are used as predictor variables for disease risk. Disease risk did not correlate with host diversity changes. However, the densities of each infected rodent species were positively associated with disease risk. We suggest that the infected host density surrounding the vector colonies is a relevant variable for disease risk and should be considered to understand disease dynamics. It is crucial to pay attention on the spatial scale of analysis, considering the pattern of vector dispersal, when the relationship between host diversity and disease risk is studied.     

Host and vector movement affects genetic diversity and spatial structure of Buggy Creek virus (Togaviridae)

Determining the degree of genetic variability and spatial structure of arthropod-borne viruses (arboviruses) may help in identifying where strains that potentially cause epidemics or epizootics occur. Genetic diversity in arboviruses is assumed to reflect relative mobility of their vertebrate hosts (and invertebrate vectors), with highly mobile hosts such as birds leading to genetic similarity of viruses over large areas. There are no empirical studies that have directly related host or vector movement to virus genetic diversity and spatial structure. Using the entire E2 glycoprotein-coding region of 377 Buggy Creek virus isolates taken from cimicid swallow bugs (Oeciacus vicarius), the principal invertebrate vector for this virus, we show that genetic diversity between sampling sites could be predicted by the extent of movement by transient cliff swallows (Petrochelidon pyrrhonota) between nesting colonies where the virus and vectors occur. Pairwise F(ST) values between colony sites declined significantly with increasing likelihood of a swallow moving between those sites per 2-day interval during the summer nesting season. Sites with more bird movement between them had virus more similar genetically than did pairs of sites with limited or no bird movement. For one virus lineage, Buggy Creek virus showed greater haplotype and nucleotide diversity at sites that had high probabilities of birds moving into or through them during the summer; these sites likely accumulated haplotypes by virtue of frequent virus introductions by birds. Cliff swallows probably move Buggy Creek virus by transporting infected bugs on their feet. The results provide the first empirical demonstration that genetic structure of an arbovirus is strongly associated with host/vector movement, and suggest caution in assuming that bird-dispersed arboviruses always have low genetic differentiation across different sites.     

Vector preference and host defense against infection interact to determine disease dynamics

Vector preference based on host infection status has long been recognized for its importance in disease dynamics. Prior theoretical work has assumed that all hosts are uniformly susceptible to the pathogen. Here we investigated disease dynamics when this assumption is relaxed using a series of vector–host epidemiological compartment models with variable levels of host resistance or tolerance to infection – collectively termed defense. In our models, vectors cannot acquire the infection from resistant hosts but can acquire from tolerant hosts. Specifically, we investigated the interacting effects of vector preference and host defense in a series of single‐ and two‐patch models. Results indicate that resistant host types generally reduce disease prevalence and pathogen spillover, independent of vector preference. The epidemiological consequences of host tolerance, however, depended on vector preference. When vectors preferred diseased hosts, tolerance reduced incidence compared to susceptible hosts; when vectors avoided diseased hosts, tolerance enhanced disease prevalence. Finally, a variation of the model that included preference‐based vector patch leaving rates suggests that both resistance and tolerance can promote pathogen spillover if vectors prefer diseased hosts, because of increased vector dispersal into susceptible patches. Collectively, we found complex, context‐dependent effects of vector preference and host defense on disease dynamics. In the context of management programs for vector‐borne diseases, managers should consider both the precise form of host defense present in a population, breed, or cultivar, as well as vector feeding behavior.     

Biological and molecular events associated with simultaneous transmission of plant viruses by invertebrate and fungal vectors

Viruses are likely to be the most dangerous parasites of living organisms because of their widespread occurrence, possible deleterious effects on their hosts and high rates of evolution. Virus host‐to‐host transmission is a critical step in the virus life cycle, because it enables survival in a given environment and efficient dissemination. As hosts of plant viruses are not mobile, these pathogens have adopted diverse transmission strategies involving various vector organisms, mainly arthropods, nematodes, fungi and protists. In nature, plants are often infected with more than one virus at a time, thereby creating potential sources for vectors to acquire and transmit simultaneously two or more viruses. Simultaneous transmission can result in multiple infections of new host plants, which become subsequent potential sources of the viruses, thus enhancing the spread of the diseases caused by these pathogens. Moreover, it can contribute to the maintenance of viral genetic diversity in the host communities. However, despite its possible significance, the problem of the simultaneous transmission of plant viruses by vectors has not been investigated in detail. In this review, the current knowledge on multiple viral transmissions by aphids, whiteflies, leafhoppers, planthoppers, nematodes and fungi is outlined.     

Effective tolerance based on resource reallocation is a virus‐specific defence in Arabidopsis thaliana

Plant viruses often harm their hosts, which have developed mechanisms to prevent or minimize the effects of virus infection. Resistance and tolerance are the two main plant defences to pathogens. Although resistance to plant viruses has been studied extensively, tolerance has received much less attention. Theory predicts that tolerance to low‐virulent parasites would be achieved through resource reallocation from growth to reproduction, whereas tolerance to high‐virulent parasites would be attained through shortening of the pre‐reproductive period. We have shown previously that the tolerance of Arabidopsis thaliana to Cucumber mosaic virus (CMV), a relatively low‐virulent virus in this host, accords to these predictions. However, whether other viruses trigger the same response, and how A. thaliana copes with highly virulent virus infections remains unexplored. To address these questions, we challenged six A. thaliana wild genotypes with five viruses with different genomic structures, life histories and transmission modes. In these plants, we quantified virus multiplication, virulence, and the effects of infection on plant growth and reproduction, and on the developmental schedule. Our results indicate that virus multiplication varies according to the virus × host genotype interaction. Conversely, effective tolerance is observed only on CMV infection, and is associated with resource reallocation from growth to reproduction. Tolerance to the other viruses is observed only in specific host–virus combinations and, at odds with theoretical predictions, is linked to longer pre‐reproductive periods. These findings only partially agree with theoretical predictions, and contribute to a better understanding of pathogenic processes in plant–virus interactions.     

The phylogenetic range of bacterial and viral pathogens of vertebrates

Many major human pathogens are multihost pathogens, able to infect other vertebrate species. Describing the general patterns of host–pathogen associations across pathogen taxa is therefore important to understand risk factors for human disease emergence. However, there is a lack of comprehensive curated databases for this purpose, with most previous efforts focusing on viruses. Here, we report the largest manually compiled host–pathogen association database, covering 2,595 bacteria and viruses infecting 2,656 vertebrate hosts. We also build a tree for host species using nine mitochondrial genes, giving a quantitative measure of the phylogenetic similarity of hosts. We find that the majority of bacteria and viruses are specialists infecting only a single host species, with bacteria having a significantly higher proportion of specialists compared to viruses. Conversely, multihost viruses have a more restricted host range than multihost bacteria. We perform multiple analyses of factors associated with pathogen richness per host species and the pathogen traits associated with greater host range and zoonotic potential. We show that factors previously identified as important for zoonotic potential in viruses—such as phylogenetic range, research effort, and being vector‐borne—are also predictive in bacteria. We find that the fraction of pathogens shared between two hosts decreases with the phylogenetic distance between them. Our results suggest that host phylogenetic similarity is the primary factor for host‐switching in pathogens.