Pathogen Life History Traits Research Articles

An Agent-Based Model Shows How Mixed Infections Drive Multiyear Pathotype Dynamics in a Plant-Virus System.

Mathematical models are widely used to understand the evolution and epidemiology of plant pathogens under a variety of scenarios. Here, we used this approach to analyze the effects of different traits intrinsic and extrinsic to plant-virus interactions on the dynamics of virus pathotypes in genetically heterogeneous plant-virus systems. For this, we propose an agent-based epidemiological model that includes epidemiologically significant pathogen life-history traits related to virulence, transmission, and survival in the environment and allows for integrating long- and short-distance transmission, primary and secondary infections, and within-host pathogen competition in mixed infections. The study focuses on the tobamovirus-pepper pathosystem. Model simulations allowed us to integrate pleiotropic effects of resistance-breaking mutations on different virus life-history traits into the net costs of resistance breaking, allowing for predictions on multiyear pathotype dynamics. We also explored the effects of two control measures, the use of host resistance and roguing of symptomatic plants, that modify epidemiological attributes of the pathogens to understand how their populations will respond to evolutionary pressures. One major conclusion points to the importance of pathogen competition within mixed-infected hosts as a component of the overall fitness of each pathogen that, thus, drives their multiyear dynamics.

Borrelia burgdorferi strain and host sex influence pathogen prevalence and abundance in the tissues of a laboratory rodent host.

Experimental infections with different pathogen strains give insight into pathogen life history traits. The purpose of the present study was to compare variation in tissue infection prevalence and spirochete abundance among strains of Borrelia burgdorferi in a rodent host (Mus musculus, C3H/HeJ). Male and female mice were experimentally infected via tick bite with one of 12 strains. Ear tissue biopsies were taken at days 29, 59 and 89 postinfection, and seven tissues were collected at necropsy. The presence and abundance of spirochetes in the mouse tissues were measured by quantitative polymerase chain reaction. To determine the frequencies of our strains in nature, their multilocus sequence types were matched to published data sets. For the infected mice, 56.6% of the tissues were infected with B.burgdorferi. The mean spirochete load in the mouse necropsy tissues varied 4.8-fold between the strains. The mean spirochete load in the ear tissue biopsies decreased rapidly over time for some strains. The percentage of infected tissues in male mice (65.4%) was significantly higher compared to female mice (50.5%). The mean spirochete load in the seven tissues was 1.5× higher in male mice compared to female mice; this male bias was 15.3× higher in the ventral skin. Across the 11 strains, the mean spirochete loads in the infected mouse tissues were positively correlated with the strain-specific frequencies in their tick vector populations. The study suggests that laboratory-based estimates of pathogen abundance in host tissues can predict the strain composition of this important tick-borne pathogen in nature.

Considering humans as habitat reveals evidence of successional disease ecology among human pathogens.

The realization that ecological principles play an important role in infectious disease dynamics has led to a renaissance in epidemiological theory. Ideas from ecological succession theory have begun to inform an understanding of the relationship between the individual microbiome and health but have not yet been applied to investigate broader, population-level epidemiological dynamics. We consider human hosts as habitat and apply ideas from succession to immune memory and multi-pathogen dynamics in populations. We demonstrate that ecologically meaningful life history characteristics of pathogens and parasites, rather than epidemiological features alone, are likely to play a meaningful role in determining the age at which people have the greatest probability of being infected. Our results indicate the potential importance of microbiome succession in determining disease incidence and highlight the need to explore how pathogen life history traits and host ecology influence successional dynamics. We conclude by exploring some of the implications that inclusion of successional theory might have for understanding the ecology of diseases and their hosts.

Alternate patterns of temperature variation bring about very different disease outcomes at different mean temperatures.

The dynamics of host-parasite interactions are highly temperature-dependent and may be modified by increasing frequency and intensity of climate-driven heat events. Here, we show that altered patterns of temperature variance lead to an almost order-of-magnitude shift in thermal performance of host and pathogen life-history traits over and above the effects of mean temperature and, moreover, that different temperature regimes affect these traits differently. We found that diurnal fluctuations of ±3°C lowered infection rates and reduced spore burden compared to constant temperatures in our focal host Daphnia magna exposed to the microsporidium parasite Ordospora colligata. In contrast, a 3-day heatwave (+6°C) did not affect infection rates, but increased spore burden (relative to constant temperatures with the same mean) at 16°C, while reducing burden at higher temperatures. We conclude that changing patterns of climate variation, superimposed on shifts in mean temperatures due to global warming, may have profound and unanticipated effects on disease dynamics.

The relationship between pathogen life-history traits and metapopulation dynamics.

Summary Plant pathogen traits, such as transmission mode and overwintering strategy, may have important effects on dispersal and persistence, and drive disease dynamics. Still, we lack insights into how life‐history traits influence spatiotemporal disease dynamics.We adopted a multifaceted approach, combining experimental assays, theory and field surveys, to investigate whether information about two pathogen life‐history traits – infectivity and overwintering strategy – can predict pathogen metapopulation dynamics in natural systems. For this, we focused on four fungal pathogens (two rust fungi, one chytrid fungus and one smut fungus) on the forest herb Anemone nemorosa.Pathogens infecting new plants mostly via spores (the chytrid and smut fungi) had higher patch occupancies and colonization rates than pathogens causing mainly systemic infections and overwintering in the rhizomes (the two rust fungi). Although the rust fungi more often occupied well‐connected plant patches, the chytrid and smut fungi were equally or more common in isolated patches. Host patch size was positively related to patch occupancy and colonization rates for all pathogens.Predicting disease dynamics is crucial for understanding the ecological and evolutionary dynamics of host–pathogen interactions, and to prevent disease outbreaks. Our study shows that combining experiments, theory and field observations is a useful way to predict disease dynamics.

Influence of Temperature and Moisture Duration on Pathogenic Life History Traits of Predominant Haplotypes of Fusarium circinatum on Pinus spp. in Spain.

Pathogen life history traits influence epidemic development and pathogen adaptive ability to interact with their hosts in different environments. Reduced traits variation may compromise pathogen evolutionary potential, which is particularly important for introduced pathogens. Fusarium circinatum (cause of pine pitch canker) is an invasive fungal pathogen in Europe, with current distribution restricted to forest stands of Pinus radiata and Pinus pinaster in northern Spain and Portugal. This study aimed to quantify pathogenic traits of Spanish isolates of F. circinatum, with two of the strains representing the two dominant haplotypes in the Spanish population. Disease severity was measured on P. radiata, analyzing the influence of temperature and moisture duration on infection as well as the influence of temperature on spore germination, sporulation, and mycelial growth. Results indicated that the isolate representing the most common haplotype caused more severe disease on P. radiata at 25 and 30°C compared with the second most common haplotype but caused less severe disease at 15°C. Spore germination was higher for the most common haplotype, which produced more spores at 20 and 25°C. The isolate showed hyphal melanization at 5°C, which has been associated with survival and may be important because no resting structures have been described for F. circinatum. Our study determined that longer moisture periods during infection result in more severe disease from 7 to 24 h, regardless of the isolate virulence. This is the first study on virulence of the most abundant haplotypes of F. circinatum in Spain as affected by temperatures and moisture.

Multi‐infections, competitive interactions, and pathogen coexistence

AbstractMultiple infections, either simultaneous or sequential, affecting a single plant or crop are now recognized to be common in plant disease epidemics. These multiple infections thus generate a range of competitive interactions (exploitation competition, apparent competition, or interference competition) that directly impact competitors’ life history traits, and hence fitness. While a theoretical framework, based primarily on three ecological theories—niche exclusion, the “tragedy of the commons”, and the virulence–transmission trade‐off, provides insights into potential outcomes of multiple infections on pathogen evolution and virulence and on disease dynamics, experimental observations, although rather rare so far, strongly suggest that unexpected outputs can also occur. This review therefore attempts to provide a comprehensive overview of both theoretical and empirical knowledge about multiple infection in plants. It highlights the need for a detailed assessment of pathogen life history traits and their modulation according to competition types, host receptivity, and pathogen life strategies for a better understanding and prediction of the evolutionary and demographic outcomes of multiple infections, as well as research questions still open in this emerging field of plant pathology.

Life history and population regulation shape demographic competence and influence the maintenance of endemic disease.

Host life history and demography play important roles in host-pathogen dynamics, by influencing the ability of hosts and their pathogens to coexist. We introduce the concept of demographic competence to describe the ability of host populations to sustain endemic infectious disease. Hosts with high demographic competence are more likely to act as keystone hosts and constitute reservoirs of infection that can spill over into other species. We propose that the pace of host life history will interact with pathogen life history to influence demographic competence. Our models demonstrate that slow-living hosts (with high survival and low recruitment rates) have greater demographic competence than fast-living hosts (with low survival and high recruitment rates) for susceptible-infected disease dynamics, although this difference is reduced when populations of slow hosts are age structured. Demographic competence is generally greater among hosts with populations regulated by survival compared to reproduction, but this difference is smallest among slow life histories and reversed for some pathogens with frequency-dependent transmission. An association between pathogen life history traits and the demographic competence of faster-living hosts also has implications for trade-offs between pathogen virulence and transmissibility. Overall, we demonstrate how host life history traits can help predict wildlife reservoirs of zoonoses and the vulnerability of populations to disease-induced extinction.

Sex, synchrony, and skin contact: integrating multiple behaviors to assess pathogen transmission risk

Abstract Direct pathogen and parasite transmission is fundamentally driven by a population’s contact network structure and its demographic composition and is further modulated by pathogen life-history traits. Importantly, populations are most often concurrently exposed to a suite of pathogens, which is rarely investigated, because contact networks are typically inferred from spatial proximity only. Here, we use 5 years of detailed observations of Indo-Pacific bottlenose dolphins (Tursiops aduncus) that distinguish between four different types of social contact. We investigate how demography (sex and age) affects these different social behaviors. Three of the four social behaviors can be used as a proxy for understanding key routes of direct pathogen transmission (sexual contact, skin contact, and aerosol contact of respiratory vapor above the water surface). We quantify the demography-dependent network connectedness, representing the risk of exposure associated with the three pathogen transmission routes, and quantify coexposure risks and relate them to individual sociability. Our results suggest demography-driven disease risk in bottlenose dolphins, with males at greater risk than females, and transmission route-dependent implications for different age classes. We hypothesize that male alliance formation and the divergent reproductive strategies in males and females drive the demography-dependent connectedness and, hence, exposure risk to pathogens. Our study provides evidence for the risk of coexposure to pathogens transmitted along different transmission routes and that they relate to individual sociability. Hence, our results highlight the importance of a multibehavioral approach for a more complete understanding of the overall pathogen transmission risk in animal populations, as well as the cumulative costs of sociality.

Role of Temperature and Coinfection in Mediating Pathogen Life-History Traits.

Understanding processes maintaining variation in pathogen life-history traits is a key challenge in disease biology, and of importance for predicting when and where risks of disease emergence are highest. Pathogens are expected to encounter tremendous levels of variation in their environment – both abiotic and biotic – and this variation may promote maintenance of variation in pathogen populations through space and time. Here, we measure life-history traits of an obligate fungal pathogen at both asexual and sexual stages under both single infection and coinfection along a temperature gradient. We find that temperature had a significant effect on all measured life-history traits while coinfection only had a significant effect on the number of sexual resting structures produced. The effect of temperature on life-history traits was both direct as well as mediated through a genotype-by-temperature interaction. We conclude that pathogen life-history traits vary in their sensitivity to abiotic and biotic variation in the environment.

A foliar disease simulation model to assist the design of new control methods against black leaf streak disease of banana

Black leaf streak disease (BLSD), caused by the fungal pathogen Mycosphaerella fijiensis, is considered as the most destructive foliar disease of banana. To advance our knowledge of the dynamics of the disease at plant scale as well as of the components of varietal resistance, we designed, calibrated and evaluated a mechanistic model to simulate the disease on a banana plant. The model runs in discrete time at plant scale and describes plant growth and pathogen dynamics under optimal epidemiological conditions. The model is divided into two modules: a deterministic plant sub-model that simulates the simplified architecture and growth of the banana, and a pathogen sub-model that simulates the detailed life cycle of the pathogen including infection, lesion growth, asexual and sexual sporulation, and the dispersal of spores on the plant. The three most influential epidemiological parameters identified by sensitivity analysis of the model (lesion growth rate, infection efficiency, and incubation period) were estimated in a Bayesian framework using Markov chain Monte Carlo methods and acquired data on the dynamics of leaf lesions under natural conditions. The posterior densities provided precise knowledge on pathogen life history traits. The evaluation of the model using an independent data set confirmed the good quality of the predictions. Simulations allowed us to evaluate the impact of host resistance components, auto-infection at plant scale, and of the leaf emergence rate, which is linked with cropping practices, on the severity of BLSD. This foliar disease simulation model will help design new methods of controlling BLSD.

Rapid and multiregional adaptation to host partial resistance in a plant pathogenic oomycete: Evidence from European populations of Plasmopara viticola, the causal agent of grapevine downy mildew

Crop pathogens evolve rapidly to adapt to their hosts. The use of crops with quantitative disease resistance is expected to alter selection of pathogen life-history traits. This may result in differential adaptation of the pathogen to host cultivars and, sometimes, to the erosion of quantitative resistance. Here, we assessed the level of host adaptation in an oomycete plant pathogenic species. We analysed the phenotypic and genetic variability of 17 Plasmopara viticola isolates collected on Vitis vinifera and 35 isolates from partially resistant varieties (Regent and genotypes carrying the Rpv1 gene). Cross-inoculation experiments assessed two components of aggressiveness and a life-history trait of the pathogen: disease severity, sporangial production and sporangia size. The results contribute evidence to the emergence of P. viticola aggressive isolates presenting a high level of sporulation on the partially resistant Regent. By contrast, no adaptation to the Rpv1 gene was found in this study. The erosion of Regent resistance may have occurred in less than 5years and at least three times independently in three distant wine-producing areas. Populations from resistant varieties showed a significant increase in sporangia production capacity, indicating an absence of fitness costs for this adaptation. The increase in the number of sporangia was correlated with a reduction in sporangia size, a result which illustrates how partial plant disease resistance can impact selection of the pathogen’s life-history traits. This case study on grapevine downy mildew shows how new plant pathogen populations emerge in agro-ecosystems by adapting to partial host resistance. This adaptive pattern highlights the need for wise management of plant partial disease resistance to ensure its sustainability over time.

What have we learned from studies of wild plant-pathogen associations?—the dynamic interplay of time, space and life-history

The interplay of host and pathogen life history traits with disease epidemiology and the selective pressures exerted on hosts drives genetic change and the long-term coevolutionary trajectories of host-pathogen associations. Many studies have addressed various aspects of the ways in which hosts and their pathogens interact but have tended to focus on individual populations, on comparisons made at single points in time, or on broader comparisons that confound patterns from different epidemiological and evolutionary units. While such studies provide valuable information, their essentially ‘static’ snap-shot nature limits the ability to interpret the nature of the underpinning coevolutionary processes. An increasing number of long-term studies involving repeat sampling of multiple interaction demes distributed across space are giving insight into the complexity of the numerical and genetic dynamics of host and pathogen interactions. These illustrate: (a) the ephemerality of disease in individual populations in contrast to its predictability at the metapopulation scale; (b) the spatial and temporal dynamics of selection ‘hot-spots’, rates of extinction and recolonization; and (c) differences in coevolutionary dynamics among demes within a metapopulation. Such long-term studies further emphasise the interplay between life history traits, time and space, and the importance of developing a framework to classify the seemingly daunting diversity of host-pathogen associations.

Shared influence of pathogen and host genetics on a trade‐off between latent period and spore production capacity in the wheat pathogen, Puccinia triticina

Crop pathogens are notorious for their rapid adaptation to their host. We still know little about the evolution of their life cycles and whether there might be trade-offs between fitness components, limiting the evolutionary potential of these pathogens. In this study, we explored a trade-off between spore production capacity and latent period in Puccinia triticina, a fungal pathogen causing leaf rust on wheat. Using a simple multivariate (manova) technique, we showed that the covariance between the two traits is under shared control of host and pathogen, with contributions from host genotype (57%), pathogen genotype (18.4%) and genotype × genotype interactions (12.5%). We also found variation in sign and strength of genetic correlations for the pathogen, when measured on different host varieties. Our results suggest that these important pathogen life-history traits do not freely respond to directional selection and that precise evolutionary trajectories are contingent on the genetic identity of the interacting host and pathogen.

Virus adaptation to quantitative plant resistance: erosion or breakdown?

Adaptation of populations to new environments is frequently costly due to trade-offs between life history traits, and consequently, parasites are expected to be locally adapted to sympatric hosts. Also, during adaptation to the host, an increase in parasite fitness could have direct consequences on its aggressiveness (i.e. the quantity of damages caused to the host by the virus). These two phenomena have been observed in the context of pathogen adaptation to host's qualitative and monogenic resistances. However, the ability of pathogens to adapt to quantitative polygenic plant resistances and the consequences of these potential adaptations on other pathogen life history traits remain to be evaluated. Potato virus Y and two pepper genotypes (one susceptible and one with quantitative resistance) were used, and experimental evolutions showed that adaptation to a quantitative resistance was possible and resulted in resistance breakdown. This adaptation was associated to a fitness cost on the susceptible cultivar, but had no consequence either in terms of aggressiveness, which could be explained by a high tolerance level, or in terms of aphid transmission efficiency. We concluded that quantitative resistances are not necessarily durable but management strategies mixing susceptible and resistant cultivars in space and/or in time should be useful to preserve their efficiency.

High levels of auto-infection in plant pathogens favour short latent periods: a theoretical approach

Auto-infection (infection arising from inoculum produced on the same host unit) is common in polycyclic plant pathogens, but often neglected in experimental and theoretical studies, which focus instead on infection of new hosts (allo-infection). Here we test the hypothesis that high auto-infection, as observed for leaf infecting fungal pathogens, could select for short latent periods. An individual-based simulation model keeps track of lesions, resulting from the spread of spores, between and within individual leaves. Linked to a trade-off between latent period and spore production capacity, as observed for Puccinia triticina on wheat, the adaptation of the latent period is analysed for different levels of auto-infection using the methods of pairwise invasibility plots. Results suggest that increased auto-infection selects for reduced latent periods. A reduction in leaf longevity also selects for reduced latent periods, which is most obvious for a relatively low ratio of auto- to allo-infection. This study is the first to consider the effect of auto-infection on the evolution of pathogen life history traits. The fact that auto-infection could drastically reduce pathogen latent periods highlights the need for more research in this area.