Transmission shifts underlie variability in population responses to Yersinia pestis infection

Host populations for the plague bacterium, Yersinia pestis, are highly variable in their response to plague ranging from near deterministic extinction (i.e., epizootic dynamics) to a low probability of extinction despite persistent infection (i.e., enzootic dynamics). Much of the work to understand this variability has focused on specific host characteristics, such as population size and resistance, and their role in determining plague dynamics. Here, however, we advance the idea that the relative importance of alternative transmission routes may vary causing shifts from epizootic to enzootic dynamics. We present a model that incorporates host and flea ecology with multiple transmission hypotheses to study how transmission shifts determine population responses to plague. Our results suggest enzootic persistence relies on infection of an off-host flea reservoir and epizootics rely on transiently maintained flea infection loads through repeated infectious feeds by fleas. In either case, early-phase transmission by fleas (i.e., transmission immediately following an infected blood meal) has been observed in laboratory studies, and we show that it is capable of driving plague dynamics at the population level. Sensitivity analysis of model parameters revealed that host characteristics (e.g., population size and resistance) vary in importance depending on transmission dynamics, suggesting that host ecology may scale differently through different transmission routes enabling prediction of population responses in a more robust way than using either host characteristics or transmission shifts alone.     

Sexual cannibalism and population viability

Some behaviours that typically increase fitness at the individual level may reduce population persistence, particularly in the face of environmental changes. Sexual cannibalism is an extreme mating behaviour which typically involves a male being devoured by the female immediately before, during or after copulation, and is widespread amongst predatory invertebrates. Although the individual‐level effects of sexual cannibalism are reasonably well understood, very little is known about the population‐level effects. We constructed both a mathematical model and an individual‐based model to predict how sexual cannibalism might affect population growth rate and extinction risk. We found that in the absence of any cannibalism‐derived fecundity benefit, sexual cannibalism is always detrimental to population growth rate and leads to a higher population extinction risk. Increasing the fecundity benefits of sexual cannibalism leads to a consistently higher population growth rate and likely a lower extinction risk. However, even if cannibalism‐derived fecundity benefits are large, very high rates of sexual cannibalism (>70%) can still drive the population to negative growth and potential extinction. Pre‐copulatory cannibalism was particularly damaging for population growth rates and was the main predictor of growth declining below the replacement rate. Surprisingly, post‐copulatory cannibalism had a largely positive effect on population growth rate when fecundity benefits were present. This study is the first to formally estimate the population‐level effects of sexual cannibalism. We highlight the detrimental effect sexual cannibalism may have on population viability if (1) cannibalism rates become high, and/or (2) cannibalism‐derived fecundity benefits become low. Decreased food availability could plausibly both increase the frequency of cannibalism, and reduce the fecundity benefit of cannibalism, suggesting that sexual cannibalism may increase the risk of population collapse in the face of environmental change.     

The evolution of parasite virulence and transmission rate in a spatially structured population

If the transmission occurs through local contact of the individuals in a spatially structured population, the evolutionarily stable (ESS) traits of parasite might be quite different from what the classical theory with complete mixing predicts. In this paper, we theoretically study the ESS virulence and transmission rate of a parasite in a lattice-structured host population, in which the host can send progeny only to its neighboring vacant site, and the transmission occurs only in between the infected and the susceptible in the nearest-neighbor sites. Infected host is assumed to be infertile. The analysis based on the pair approximation and the Monte Carlo simulation reveal that the ESS transmission rate and virulence in a lattice-structured population are greatly reduced from those in completely mixing population. Unlike completely mixing populations, the spread of parasite can drive the host to extinction, because the local density of the susceptible next to the infected can remain high even when the global density of host becomes very low. This demographic viscosity and group selection between self-organized spatial clusters of host individuals then leads to an intermediate ESS transmission rate even if there is no tradeoff between transmission rate and virulence. The ESS transmission rate is below the region of parasite-driven extinction by a finite amount for moderately large reproductive rate of host; whereas, the evolution of transmission rate leads to the fade out of parasite for small reproductive rate, and the extinction of host for very large reproductive rate.     

Testing a key assumption of host‐pathogen theory: density and disease transmission

Conventional disease theory suggests that extinction with density‐dependent transmission is unlikely as the threshold host density (KT) is greater than zero. Extinction may result if transmission is frequency dependent or the pathogen has an environmental reservoir. Given the importance of understanding how pathogens affect species richness and diversity there are few empirical tests of these conclusions. We used an Ambystoma tigrinum–Ambystoma tigrinum virus (ATV) model system in the laboratory to examine disease transmission dynamics. Susceptible A. tigrinum larvae were exposed to three different densities and proportions of infected larvae for 24 h. We then housed susceptible hosts individually for 28 days and monitored them for infection. The density of infected hosts to which susceptible hosts were exposed was the best predictor of infection (p=0.037). There was no effect of host clutch on the probability of becoming infected (p=0.67). Larvae in the highest density treatments died sooner than larvae in lower density treatments (p<0.001). Asymptomatic but infected hosts shed sufficient virus into the water in a 24‐h period to infect susceptible hosts without any direct contact between individuals. ATV transmission was best described by a power function, leading to the prediction that extinction of A. tigrinum as a result of this pathogen is unlikely. Indeed, field observations show that larval salamander populations that experience ATV‐driven epidemics may decrease, but not to extinction, and then recover. Disease is proposed as a possible explanation for the global decline of amphibians. Ranaviruses infect many amphibian populations, but based on our results may not be a general cause of declines to extinction. In contrast, frequency dependent transmission, environmental reservoirs and alternative hosts may be the most likely explanation for the enigmatic decline, at times to extinction, of some amphibian populations as a result of emerging infectious diseases, like the chytrid fungus Batrachochytrium dendrobatidis.     

Parasite transmission and cannibalism in an amphipod (Crustacea)

In its freshwater amphipod host Gammarus duebeni celticus, the microsporidian parasite Pleistophora mulleri showed 23% transmission efficiency when uninfected individuals were fed infected tissue, but 0% transmission by water-borne and coprophagous routes. Cannibalism between unparasitised and parasitised individuals was significantly in favour of the former (37% compared to 0%). In addition, cannibalism between parasitised individuals was significantly higher than between unparasitised individuals (27% compared to 0%). Thus, parasitised individuals were more likely to be cannibalised by both unparasitised and parasitised individuals. We discuss the conflicting selective forces within this host/parasite relationship, the implications of parasite mediated cannibalism for host population structure and the impacts this may have on the wider aquatic community.     

Haemoplasmas in wild rodents: Routes of transmission and infection dynamics

The way that some parasites and pathogens persist in the hostile environment of their host for long periods remains to be resolved. Here, longitudinal field surveys were combined with laboratory experiments to investigate the routes of transmission and infection dynamics of such a pathogen—a wild rodent haemotropic bacterium, specifically a Mycoplasma haemomuris‐like bacterium. Fleaborne transmission, direct rodent‐to‐rodent transmission and vertical transmission from fleas or rodents to their offspring were experimentally quantified, and indications were found that the main route of bacterial transmission is direct, although its rate of successful transmission is low (~20%). The bacterium's temporal dynamics was then compared in the field to that observed under a controlled infection experiment in field‐infected and laboratory‐infected rodents, and indications were found, under all conditions, that the bacterium reached its peak infection level after 25–45 days and then decreased to low bacterial loads, which persist for the rodent's lifetime. These findings suggest that the bacterium relies on persistency with low bacterial loads for long‐term coexistence with its rodent host, having both conceptual and applied implications.     

Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus

Transmission is central to pathogen fitness and strongly influences the impact of pathogens on host populations. Particularly important to transmission dynamics is the distinction between direct transmission requiring close physical contact (e.g. bumping, fighting, or coughing) and indirect transmission from environmental sources such as contaminated substrates. We present data from 4 experiments addressing the form, routes, and timing of transmission of Ambystoma tigrinum virus (ATV) among tiger salamanders Ambystoma tigrinum nebulosum. Our data suggest that ATV is efficiently transmitted by direct interactions between live animals (bumping, biting and cannibalism) as well as by necrophagy and indirectly via water and fomites. Determining which form of transmission is most important in nature is essential for understanding transmission at the population level. Our experiments also revealed an important temporal aspect of infectiousness: larval salamanders become infectious soon after exposure to ATV and their propensity to infect others increases with time. These results begin to clarify the mechanisms and dynamics of ATV transmission and lead to key questions that need to be addressed in future research.     

Virulence and transmission modes in metapopulations: when group selection increases virulence

Individuals that are infected by a pathogen can transmit it to unrelated conspecifics (horizontal transmission) or to their progeny when they reproduce (vertical transmission). The mechanisms of these two routes of transmission are different and this difference impacts the way virulence evolves in pathogens. More precisely, horizontal transmission depends on the probability that an infected host contacts susceptible conspecifics, and therefore on its lifespan. Vertical transmission additionally depends on the host's fecundity. This additional dependence in vertically transmitted pathogens results in a decrease in their evolutionarily stable (ES) virulence.Spatial structure is another factor that is often supposed to decrease pathogens’ ES virulence, mostly because it impedes competition for transmission in local populations of hosts. In this paper, using the adaptive dynamics framework, we show that spatial structure can increase ES virulence when pathogens are mostly vertically transmitted. This is due to the difference in how pathogens compete for transmission in local population of hosts, depending on how they are transmitted. We also show that symbionts that are horizontally transmitted should respond more to a change in spatial structure than symbionts that are vertically transmitted.     

Resistance,tolerance and environmental transmission dynamics determine host extinction risk in a load‐dependent amphibian disease

While disease‐induced extinction is generally considered rare, a number of recently emerging infectious diseases with load‐dependent pathology have led to extinction in wildlife populations. Transmission is a critical factor affecting disease‐induced extinction, but the relative importance of transmission compared to load‐dependent host resistance and tolerance is currently unknown. Using a combination of models and experiments on an amphibian species suffering extirpations from the fungal pathogen Batrachochytrium dendrobatidis (Bd), we show that while transmission from an environmental Bd reservoir increased the ability of Bd to invade an amphibian population and the extinction risk of that population, Bd‐induced extinction dynamics were far more sensitive to host resistance and tolerance than to Bd transmission. We demonstrate that this is a general result for load‐dependent pathogens, where non‐linear resistance and tolerance functions can interact such that small changes in these functions lead to drastic changes in extinction dynamics.     

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.     

Modelling Fungal (Neozygites cf. Floridana) Epizootics in Local Populations of Cassava Green Mites (Mononychellus Tanajoa)

The fungus, Neozygitis cf. floridana is parasitic on the cassava green mite, Mononychellus tanajoa (Bondar) (Acari: Tetranychidae) in South America and may be considered for classical biological control of cassava green mites in Africa, where cassava is an important subsistence crop, cassava green mites are an imported pest and specific natural enemies are lacking. Spider mites generally have a viscous structure of local populations, a trait that would normally hamper the spread of a fungus that is transmitted by the contact of susceptible hosts with the halo of capilliconidia surrounding an infectious host. However, if infected mites search and settle to produce capilliconidia on sites where they are surrounded by susceptible mites before becoming infectious, then the conditions for maximal transmission in a viscous host population are met. Because the ratio between spider mites and the leaf area they occupy is constant, parasite-induced host searching behaviour leads to a constant per capita transmission rate. Hence, the transmission rate only depends on the number of infectious hosts. These assumptions on parasite-induced host search and constant host density lead to a simple, analytically tractable model that can be used to estimate the maximal capacity of the fungus to decimate local populations of the cassava green mite. By estimating the parameters of this model (host density, per capita transmission rate and duration of infected and infectious state) it was shown that the fungal pathogen can reduce the population growth of M. tanajoa, but cannot drive local mite populations to extinction. Only when the initial ratio of infectious to susceptible mites exceeds unity or the effective growth rate of the mite population is sufficiently reduced by other factors than the fungus (e.g. lower food quality of the host plant, dislodgement and death by rain and wind and predation), will the fungal pathogen be capable of decimating the cassava green mite population. Under realistic field conditions, where all of these growth-reducing factors are likely to operate, there may well be room for effective control by the parasitic fungus. This revised version was published online in November 2006 with corrections to the Cover Date.     

The crayfish plague pathogen can infect freshwater‐inhabiting crabs

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Host genetics and pathogen species modulate infection-induced changes in social aggregation behaviour

Identifying how infection modifies host behaviours that determine social contact networks is important for understanding heterogeneity in infectious disease dynamics. Here, we investigate whether group social behaviour is modified during bacterial infection in fruit flies (Drosophila melanogaster) according to pathogen species, infectious dose, host genetic background and sex. In one experiment, we find that systemic infection with four different bacterial species results in a reduction in the mean pairwise distance within infected female flies, and that the extent of this change depends on pathogen species. However, susceptible flies did not show any evidence of avoidance in the presence of infected flies. In a separate experiment, we observed genetic- and sex-based variation in social aggregation within infected, same-sex groups, with infected female flies aggregating more closely than infected males. In general, our results confirm that bacterial infection induces changes in fruit fly behaviour across a range of pathogen species, but also highlight that these effects vary between fly genetic backgrounds and can be sex-specific. We discuss possible explanations for sex differences in social aggregation and their consequences for individual variation in pathogen transmission.     

Neotyphodium endophyte infection frequency in annual grass populations: relative importance of mutualism and transmission efficiency

Persistence and ubiquity of vertically transmitted Neotyphodium endophytes in grass populations is puzzling because infected plants do not consistently exhibit increased fitness. Using an annual grass population model, we show that the problems for matching endophyte infection and mutualism are likely to arise from difficulties in detecting small mutualistic effects, variability in endophyte transmission efficiency and an apparent prevalence of non-equilibrium in the dynamics of infection. Although endophytes would ultimately persist only if the infection confers some fitness increase to the host plants, such an increase can be very small, as long as the transmission efficiency is sufficiently high. In addition, imperfect transmission limits effectively the equilibrium infection level if the infected plants exhibit small or large reproductive advantage. Under frequent natural conditions, the equilibrium infection level is very sensitive to small changes in transmission efficiency and host reproductive advantage, while convergence to such an equilibrium is slow. As a consequence, seed immigration and environmental fluctuation are likely to keep local infection levels away from equilibrium. Transient dynamics analysis suggests that, when driven by environmental fluctuation, infection frequency increases would often be larger than decreases. By contrast, when due to immigration, overrepresentation of infected individuals tends to vanish faster than equivalent overrepresentation of non-infected individuals.     

Niche‐based host extinction increases prevalence of an environmentally acquired pathogen

Understanding the ecology of environmentally acquired and multi‐host pathogens affecting humans and wildlife has been elusive in part because fluctuations in the abundance of host and pathogen species may feed back onto pathogen transmission. Complexity of pathogen‐host dynamics emerges from processes driving local extinction of the pathogen, its hosts and non‐hosts. While the extinction of species may entail losses in pathogen–host interactions and decrease the proportion of hosts infected by a pathogen (prevalence), some studies suggest the opposite pattern. Niche‐based extinction, based on the species tolerance to environmental conditions, may increase prevalence of infection because the pathogen and its hosts persist, while other species go extinct. Hence, understanding prevalence of infection requires disentangling random‐ and niche‐based extinction processes occurring simultaneously. To contribute to this exercise, we analysed the prevalence of an environmentally acquired, multi‐host pathogen, Mycobacterium ulcerans (MU), in a unique dataset of 16 communities of freshwater animals, surveyed during 12 months in Akonolinga, Cameroon in equatorial Africa. Two different ecosystems were identified: rivers (lotic) and swamps and flooded areas (lentic). Increased prevalence of MU infection was correlated with niche‐based extinction of aquatic host invertebrates and vertebrates in the lentic ecosystems, whereas decreased prevalence was associated with random disassembly of the lotic ecosystems. This finding suggests that random and niche‐based extinction of host taxa are key to assessing the effect of local extinction of species on the ecology of environmentally acquired and multi‐host pathogens.     

Modelling contact spread of infection in host-parasitoid systems: Vertical transmission of pathogens can cause chaos

All animals and plants are, to some extent, susceptible to disease caused by varying combinations of parasites, viruses and bacteria. In this paper, we develop a mathematical model of contact spread infection to investigate the effect of introducing a parasitoid-vectored infection into a one-host-two-parasitoid competition model. We use a system of ordinary differential equations to investigate the separate influences of horizontal and vertical pathogen transmission on a model system appropriate for a variety of competitive situations. Computational simulations and steady-state analysis show that the transient and long-term dynamics exhibited under contact spread infection are highly complex. Horizontal pathogen transmission has a stabilising effect on the system whilst vertical transmission can destabilise it to the point of chaotic fluctuations in population levels. This has implications when considering the introduction of host pathogens for the control of insect vectored diseases such as bovine tuberculosis or yellow fever.     

How should environmental stress affect the population dynamics of disease?

We modelled how stress affects the population dynamics of infectious disease. We were specifically concerned with stress that increased susceptibility of uninfected hosts when exposed to infection. If such stresses also reduced resources, fecundity and/or survivorship, there was a reduction in the host carrying capacity. This lowered the contact between infected and uninfected hosts, thereby decreasing transmission. In addition, stress that increased parasite mortality decreased disease. The opposing effects of stress on disease dynamics made it difficult to predict the response of disease to environmental stress. We found analytical solutions with negative, positive, convex and concave associations between disease and stress. Numerical simulations with randomly generated parameter values suggested that the impact of host‐specific diseases generally declined with stress while the impact of non‐specific (or open) diseases increased with stress. These results help clarify predictions about the interaction between environmental stress and disease in natural populations.     

Populations and infectious diseases: Dynamics and evolution

The host-parasite or host-pathogen system was analyzed from dynamical and evolutionary viewpoints using simple mathematical models incorporating vertical transmission, immunity and its loss. We first analyzed a model without density regulation of host population. In the analysis on dynamics, the condition for the pathogen to work as a density regulating factor was obtained. In the analysis on evolution, criteria for the evolution of host and pathogen were proposed. These criteria implies that the evolution of hosts should result in an increase in infected host density, whereas the evolution of pathogens a decrease in susceptible host density. The direction of evolution at some parameters of host and that of pathogen were examined when the parameters were independently and freely changeable. Among the parameters, only reduction in additional mortality due to infection was the evolutionary trend common to both host and pathogen. In all the other parameters examined, trend of evolution predicted in host is reversed in pathogen. We then analyzed whether the obtained criteria still hold in models with density regulation of hosts. Using randomly generated parameter sets, we obtained the result that the criteria should hold very likely though they do not always hold. We discussed evolution of virulence when there is a constraint between the traits.     

Pathogen invasion and host extinction in lattice structured populations

We examined the propagation of an infectious disease and the eventual extinction of the host population in a lattice-structured population. Both the host colonization and pathogen transmission processes are assumed to be restricted to act between the nearest neighbor sites. The model is analyzed by an improved version of pair approximation (IPA). Pair approximation is a technique to trace the dynamics of the number of nearest neighbor pairs having particular states, and IPA takes account of the clustering property of lattice models more precisely. The results are checked by computer simulations. The analysis shows: (i) in a one-dimensional lattice population, a pathogen cannot invade a host population no matter how large is the transmission rate; (ii) in a two-dimensional lattice population, pathogens will drive the host to extinction if the transmission rate is larger than a threshold. These results indicate that spatially structured population models may give qualitatively different results from conventional population models, such as Lotka-Volterra ones, without spatial structure.     

Mechanistic models can reveal infection pathways from prevalence data: the mysterious case of polar bears Ursus maritimus and Trichinella nativa

Parasites exhibit a diverse range of life history strategies. Transmission to a host is a key component of each life cycle but the difficulty of observing host–parasite contacts has often led to confusion surrounding transmission pathways. Given limited data on most host–parasite systems, flexible approaches are needed for disentangling the obscure transmission dynamics of these systems. Here, we develop a modelling framework for formally testing long-standing hypotheses regarding how the parasitic nematode Trichinella nativa is maintained at high prevalences in polar bear populations. We evaluated transmission from marine prey, from scavenging terrestrial carrion, from cannibalism and from scavenging on dead infected bears as possible pathways, and assessed their respective importance by comparing model-projected prevalences for each mechanism against observed total and age-specific population prevalences in the Southern Beaufort Sea polar bear subpopulation. Cannibalism and the scavenging on conspecifics have previously been assumed to be critical transmission pathways, but despite data scarcity, our model exposes these mechanisms as ineffective across a wide range of plausible parameter values. Instead, our analyses suggest that transmission from the consumption of infected marine prey, and in particular seals, can explain observed prevalence levels by itself, with other transmission pathways likely playing varying small contributing roles. Furthermore, our model suggests that transmission declines with bear age, perhaps due to age-dependent changes in diet or immunity. By formalising multiple transmission mechanisms in a unified, mathematical framework, we distilled several hypotheses to a likely main mode of T. nativa transmission to polar bears. The specifics of our model are tailored towards the T. nativa-polar bear system, but the approach is easily generalized; it provides a powerful, quantitative means for ecologists to explore competing hypothesis for parasite transmission and other difficult-to-observe animal interactions even in data-poor systems.