Effects of host heterogeneity on pathogen diversity and evolution

Phenotypic variation is common in most pathogens, yet the mechanisms that maintain this diversity are still poorly understood. We asked whether continuous host variation in susceptibility helps maintain phenotypic variation, using experiments conducted with a baculovirus that infects gypsy moth (Lymantria dispar) larvae. We found that an empirically observed tradeoff between mean transmission rate and variation in transmission, which results from host heterogeneity, promotes long‐term coexistence of two pathogen types in simulations of a population model. This tradeoff introduces an alternative strategy for the pathogen: a low‐transmission, low‐variability type can coexist with the high‐transmission type favoured by classical non‐heterogeneity models. In addition, this tradeoff can help explain the extensive phenotypic variation we observed in field‐collected pathogen isolates, in traits affecting virus fitness including transmission and environmental persistence. Similar heterogeneity tradeoffs might be a general mechanism promoting phenotypic variation in any pathogen for which hosts vary continuously in susceptibility.     

The effect of land type diversity and spatial heterogeneity on farmland birds in Norway

The decline in farmland birds observed throughout Europe during recent decades has attracted much attention. Agricultural intensification or land abandonment are commonly forwarded as key drivers. Several countries have established agri-environmental schemes (AES) to counter these negative trends among farmland birds. This paper reports a study of the relationship between land use and bird species in the agricultural landscape of Norway. The main objective was to investigate the effect of spatial heterogeneity and diversity of land use on total richness and abundance of farmland birds at a national level.Monitoring the distribution and abundance of birds is part of the Norwegian monitoring programme for agricultural landscapes. The monitoring programme is based on mapping of 1 × 1 km squares distributed across the entire agricultural landscape. Within these squares permanent observation points are established for bird monitoring. Detailed interpretation of aerial photographs provides the land classification. We tested the relationship between landscape metrics at different levels of land type detail and species richness and abundance of farmland and non-farmland birds.There was a positive relationship between species richness and abundance of farmland birds and agricultural area. For non-farmland birds the relationship was negative. Spatial heterogeneity of land use was a significant positive factor for both farmland and non-farmland species. High land type diversity was positive for farmland bird richness, but negative for abundance. Non-farmland bird richness was not affected by land type diversity, but abundance had a negative response.The results presented in this paper highlight the importance of a spatial heterogeneous landscape. However, we also found that land type diversity could negatively affect the abundance of both farmland and non-farmland birds. Our findings suggest a need for different management approaches depending on whether the aim is increased species richness or abundance. Achieving both aims with the same means might be difficult. We thus suggest a need for land use analyses before proper management strategies can be implemented.     

The evolution of host specialisation in avian brood parasites

Traditional ecological theory predicts that specialisation can promote speciation; hence, recently derived species are specialists. However, an alternative view is that new species have broad niches, which become narrower and specialised over time. Here, we test these hypotheses using avian brood parasites and three different measures of host specialisation. Brood parasites provide an ideal system in which to investigate the evolution of specialisation, because some exploit more than 40 host species and others specialise on only one. We find that young brood parasite species are smaller and specialise on a narrower range of host sizes, as expected, if specialisation is linked with the generation of new species. Moreover, we show that highly virulent parasites are more specialised, supporting findings in other host–parasite systems. Finally, we demonstrate that different measures of specialisation can lead to different conclusions, and specialisation indices should be designed taking into account the biology of each system.     

The evolution of host protection by vertically transmitted parasites

Hosts are often infected by a variety of different parasites, leading to competition for hosts and coevolution between parasite species. There is increasing evidence that some vertically transmitted parasitic symbionts may protect their hosts from further infection and that this protection may be an important reason for their persistence in nature. Here, we examine theoretically when protection is likely to evolve and its selective effects on other parasites. Our key result is that protection is most likely to evolve in response to horizontally transmitted parasites that cause a significant reduction in host fecundity. The preponderance of sterilizing horizontally transmitted parasites found in arthropods may therefore explain the evolution of protection seen by their symbionts. We also find that protection is more likely to evolve in response to highly transmissible parasites that cause intermediate, rather than high, virulence (increased death rate when infected). Furthermore, intermediate levels of protection select for faster, more virulent horizontally transmitted parasites, suggesting that protective symbionts may lead to the evolution of more virulent parasites in nature. When we allow for coevolution between the symbiont and the parasite, more protection is likely to evolve in the vertically transmitted symbionts of longer lived hosts. Therefore, if protection is found to be common in nature, it has the potential to be a major selective force on host–parasite interactions.     

The role of trade-off shapes in the evolution of parasites in spatial host populations: an approximate analytical approach

Given the substantial changes in mixing in many populations, there is considerable interest in the role that spatial structure can play in the evolution of disease. Here we examine the role of different trade-off shapes in the evolution of parasites in a spatially structured host population where infection can occur locally or globally. We develop an approximate adaptive dynamic analytical approach, to examine how the evolutionarily stable (ES) virulence depends not only on the fraction of global infection/transmission but also on the shape of the trade-off between transmission and virulence. Our analysis can successfully predict the ES virulence found previously by simulation of the full system. The analysis confirms that when there is a linear trade-off between transmission and virulence spatial structure may lead to an ES virulence that increases as the proportion of global transmission increases. However, we also show that the ESS disappears above a threshold level of global infection, leading to maximization. In addition just below this threshold, there is the possibility of evolutionary bi-stabilities. When we assume the realistic trade-off between transmission and virulence that results in an ESS in the classical mixed model, we find that spatial structure can increase or decrease the ES virulence. A relatively high proportion of local infection reduces virulence but intermediate levels can select for higher virulence. Our work not only emphasizes the importance of spatial structure to the evolution of parasites, but also makes it clear that situations between the local and the global need to be considered. We also emphasize the key role that the shape of trade-offs plays in evolutionary outcomes.     

The effect of grazing on the spatial heterogeneity of vegetation

Grazing can alter the spatial heterogeneity of vegetation, influencing ecosystem processes and biodiversity. Our objective was to identify why grazing causes increases in the spatial heterogeneity of vegetation in some cases, but decreases in others. The immediate effect of grazing on heterogeneity depends on the interaction between the spatial pattern of grazing and the pre-existing spatial pattern of vegetation. Depending on the scale of observation and on the factors that determine animal distribution, grazing patterns may be stronger or weaker than vegetation patterns, or may mirror the spatial structure of vegetation. For each possible interaction between these patterns, we make a prediction about resulting changes in the spatial heterogeneity of vegetation. Case studies from the literature support our predictions, although ecosystems characterized by strong plant-soil interactions present important exceptions. While the processes by which grazing causes increases in heterogeneity are clear, how grazing leads to decreases in heterogeneity is less so. To explore how grazing can consistently dampen the fine-scale spatial patterns of competing plant species, we built a cell-based simulation model that features two competing plant species, different grazing patterns, and different sources of vegetation pattern. Only the simulations that included neighborhood interactions as a source of vegetation pattern produced results consistent with the predictions we derived from the literature review.     

The impact of host genetic diversity on virus evolution and emergence

Accumulating evidence indicates that biodiversity has an important impact on parasite evolution and emergence. The vast majority of studies in this area have only considered the diversity of species within an environment as an overall measure of biodiversity, overlooking the role of genetic diversity within a particular host species. Although theoretical models propose that host genetic diversity in part shapes that of the infecting parasite population, and hence modulates the risk of parasite emergence, this effect has seldom been tested empirically. Using Rabies virus (RABV) as a model parasite, we provide evidence that greater host genetic diversity increases both parasite genetic diversity and the likelihood of a host being a donor in RABV cross‐species transmission events. We conclude that host genetic diversity may be an important determinant of parasite evolution and emergence.     

The role of host population heterogeneity in the evolution of virulence

I examine here the effects of host heterogeneity in the growth of immune response on the evolution and co-evolution of virulence. The analysis is based on an extension of the 'nested model' by Gilchrist and Sasaki [Modeling host-parasite coevolution, J. Theor. Biol. 218 (2002), pp. 289-308]; the criteria for host and parasite evolution, in the paradigm of adaptive dynamics, for that model are derived in generality. Host heterogeneity is assumed to be fixed at birth according to a lognormal distribution or to the presence of two discrete types. In both cases, it is found that host heterogeneity determines a dramatic decrease in pathogen virulence, since pathogens will tune to the 'weakest' hosts. Finally we clarify how contrasting results present in the literature are due to different modelling assumptions.     

The evolution of virulence and host specialization in malaria parasites of primates

Parasite virulence, i.e. the damage done to the host, may be a by-product of the parasite's effort to maximize its fitness. Accordingly, several life-history trade-offs may explain interspecific differences in virulence, but such constraints remain little tested in an evolutionary context. In this phylogenetic study of primate malarias, I investigated the relationship between virulence and other parasite life-history traits. I used peak parasitaemia as a proxy for virulence, because it reflected parasite reproductive success and parasite-induced mortality. Peak parasitaemia was higher in specialist than in generalist species, even when confounding life-history traits were controlled. While there was a significant phylogenetic relationship between the number of competitors per host and host specialization, peak parasitaemia was unrelated to within-host competition. Therefore, the key evolutionary factor that favours virulence is host specialization, and the evolutionary success of virulent parasites, such as Plasmodium falciparum , may be better understood when the trade-off in virulence between different hosts is considered. Such phylogenetic results may help us design better protection programmes against malaria.     

Deterministic extinction effect of parasites on host populations

 Experimental studies have shown that parasites can reduce host density and even drive host population to extinction. Conventional mathematical models for parasite-host interactions, while can address the host density reduction scenario, fail to explain such deterministic extinction phenomena. In order to understand the parasite induced host extinction, Ebert et al. (2000) formulated a plausible but ad hoc epidemiological microparasite model and its stochastic variation. The deterministic model, resembles a simple SI type model, predicts the existence of a globally attractive positive steady state. Their simulation of the stochastic model indicates that extinction of host is a likely outcome in some parameter regions. A careful examination of their ad hoc model suggests an alternative and plausible model assumption. With this modification, we show that the revised parasite-host model can exhibit the observed parasite induced host extinction. This finding strengthens and complements that of Ebert et al. (2000), since all continuous models are likely break down when all population densities are small. This extinction dynamics resembles that of ratio-dependent predator-prey models. We report here a complete global study of the revised parasite-host model. Biological implications and limitations of our findings are also presented. Received: 30 October 2001 / Revised version: 11 February 2002 / Published online: 17 October 2002 Work is partially supported by NSF grant DMS-0077790 Mathematics Subject Classification (2000): 34C25, 34C35, 92D25. Keywords or phrases: Microparasite model – Ratio-dependent predator-prey model – Host extinction – Global stability – Biological control     

Origins and evolution of antigenic diversity in malaria parasites

Each year, malaria parasites cause more than 500 million infections and 0.5-3 million deaths worldwide, mostly among children under five living in sub-Saharan Africa. In contrast with several viral and bacterial pathogens, which elicit long-lived immunity after a primary infection, these parasites require several years of continuous exposure to confer partial, usually non-sterilizing immune protection. One of the main obstacles to the acquisition of antimalarial immunity is the high degree of antigenic diversity in potential target antigens, which enables parasites to evade immune responses elicited by past exposure to variant forms of the same antigen. Allelic polymorphism, the existence of genetically stable alternative forms of antigen-coding genes, originates from nucleotide replacement mutations and intragenic recombination. In addition, malaria parasites display antigenic variation, whereby a clonal lineage of parasites expresses successively alternate forms of an antigen without changes in genotype. This review focuses on molecular and evolutionary processes that promote allelic polymorphism and antigenic variation in natural malaria parasite populations and their implications for naturally acquired immunity and vaccine development.     

The effect of spatial heterogeneity on the persistence of predator-prey interactions

The effect of spatially discontinuous environments on predator-prey systems is examined by using a computer simulation model. It is shown that increasing prey dispersal and decreasing predator dispersal do not necessarily have a stabilizing influence on the interaction, as had been concluded by previous workers. The stability of predator-prey interaction depends on the interaction of the dispersal process with normal reproduction and feeding of the predator and prey species.     

Competition promotes the evolution of host generalists in obligate parasites

Ecological theory traditionally predicts that interspecific competition selects for an increase in ecological specialization. Specialization, in turn, is often thought to be an evolutionary ‘dead end,’ with specialist lineages unlikely to evolve into generalist lineages. In host–parasite systems, this specialization can take the form of host specificity, with more specialized parasites using fewer hosts. We tested the hypothesis that specialists are evolutionarily more derived, and whether competition favours specialization, using the ectoparasitic feather lice of doves. Phylogenetic analyses revealed that complete host specificity is actually the ancestral condition, with generalists repeatedly evolving from specialist ancestors. These multiple origins of generalists are correlated with the presence of potentially competing species of the same genus. A competition experiment with captive doves and lice confirmed that congeneric species of lice do, in fact, have the potential to compete in ecological time. Taken together, these results suggest that interspecific competition can favour the evolution of host generalists, not specialists, over macroevolutionary time.     

The effect of partial host immunity on the transmission of malaria parasites.

Experiments were carried out to determine the effect of partial host immunity against the rodent malaria parasite Plasmodium chabaudi on the transmission success of the parasite. There was a fourfold reduction in both the blood-stage, asexually replicating parasite density and the gametocyte (transmissable stage) density in immunized hosts. Some of the reduction in asexual parasite densities was due to strain-specific immunity, but there was no evidence that strain-specific immunity affected gametocyte densities. However, immunity did affect transmission in a strain-specific manner, with a fivefold reduction in gametocyte infectivity to mosquitoes in homologous challenges compared with heterologous challenges or non-immunized controls. This implies the existence of a mechanism of strain-specific infectivity-reducing immunity that does not affect the density of gametocytes circulating in peripheral blood. The proportion of asexual parasites that produced gametocytes increased during the course of infection in both non-immunized and in immunized hosts, but immunity increased gametocyte production early in the infection.     

Short-term rates of parasite evolution predict the evolution of host diversity

Coevolution with parasites has been implicated as an important factor driving the evolution of host diversity. Studies to date have focussed on gross effects of parasites: how host diversity differs in the presence vs. absence of parasites. But parasite-imposed selection is likely to show rapid variation through time. It is unclear whether short-term fluctuations in the strength of parasite-imposed selection tend to affect host diversity, because increases in host diversity are likely to be constrained by both the supply of genetic variation and ecological processes. We followed replicate populations of coevolving, initially isogenic, bacteria and phages through time, measuring host diversity (with respect to bacterial colony morphologies), host density and rates of parasite evolution. Both host density and time-lagged rates of parasite evolution were good independent predictors of the magnitude of bacterial within- and between-population diversities. Rapid parasite evolution and low host density decreased host within-population diversity, but increased between-population diversity. This study demonstrates that short-term changes in the rate of parasite evolution can predictably drive patterns of host diversity.     

Differential sources of host species heterogeneity influence the transmission and control of multihost parasites

Controlling parasites that infect multiple host species often requires targeting single species that dominate transmission. Yet, it is rarely recognised that such ‘key hosts’ can arise through disparate mechanisms, potentially requiring different approaches for control. We identify three distinct, but not mutually exclusive, processes that underlie host species heterogeneity: infection prevalence, population abundance and infectiousness. We construct a theoretical framework to isolate the role of each process from ecological data and to explore the outcome of different control approaches. Applying this framework to data on 11 gastrointestinal parasites in small mammal communities across the eastern United States reveals variation not only in the magnitude of transmission asymmetries among host species but also in the processes driving heterogeneity. These differences influence the efficiency by which different control strategies reduce transmission. Identifying and tailoring interventions to a specific type of key host may therefore enable more effective management of multihost parasites.     

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.     

The evolution of host manipulation by parasites: a game theory analysis

Many parasites are known to manipulate the behaviour of intermediate hosts in order to increase their probability of transmission to definitive hosts. This manipulation must have costs. Here we explore the combined effects of three such costs on the amount of effort a parasite should expend on host manipulation. Manipulation can have direct costs to future reproductive success due to energy expended to manipulate the host. There may also be indirect costs if other parasites infect the host and profit from the manipulation without paying the cost of manipulation. These “free riders” may impose a third cost by competing with manipulators for resources within the host. Using game theory analysis and several different competition models we show that intrahost competition will decrease the investment that a parasite should make in manipulation but that manipulation can, under some circumstances, be a profitable strategy even in the presence of non-manipulating competitors. The key determinants of the manipulator’s success and its investment in manipulation are the relatedness among parasites within the host, the ratio of the passive transmission rate to the efficiency of increasing transmission rate and the strength of competitive effects. Manipulation, when exploited by others, becomes an altruistic behaviour. Thus we suggest that our model may be generally applicable to cases where organisms can exploit the investment of others (possibly kin) while also competing with the organism whose investment they exploit.     

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.