Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

Clerc, Melanie; Ebert, Dieter; Hall, Matthew D.

doi:10.1098/rspb.2014.2820

Cited by 48 publications

(92 citation statements)

References 42 publications

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“…P. ramosa Metchnikoff is a common Gram‐positive bacterial pathogen of D. magna found across the Northern Hemisphere (Ebert et al, ). During the course of infection, P. ramosa supresses reproduction of its host, causes pathogen‐induced gigantism and severely reduces host lifespan, before releasing millions of spores into the environment at host death (Clerc et al, ; Ebert et al, ; Hall & Ebert, ). Thus, transmission is exclusively horizontal in this system and depends on a balance between the virulence of the pathogen and its production of mature transmission spores (see Hall & Mideo, ).…”

Section: Methodsmentioning

confidence: 99%

Pathogen exposure disrupts an organism's ability to cope with thermal stress

Hector

Sgrò

Hall

2019

Global Change Biology

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As a result of global climate change, species are experiencing an escalation in the severity and regularity of extreme thermal events. With patterns of disease distribution and transmission predicted to undergo considerable shifts in the coming years, the interplay between temperature and pathogen exposure will likely determine the capacity of a population to persist under the dual threat of global change and infectious disease. In this study, we investigated how exposure to a pathogen affects an individual's ability to cope with extreme temperatures. Using experimental infections of Daphnia magna with its obligate bacterial pathogen Pasteuria ramosa, we measured upper thermal limits of multiple host and pathogen genotype combinations across the dynamic process of infection and under various forms (static and ramping) of thermal stress. We find that pathogens substantially limit the thermal tolerance of their host, with the reduction in upper thermal limits on par with the breadth of variation seen across similar species entire geographical ranges. The precise magnitude of any reduction, however, was specific to the host and pathogen genotype combination. In addition, as thermal ramping rate slowed, upper thermal limits of both healthy and infected individuals were reduced. Our results suggest that the capacity of a population to evolve new thermal limits, when also faced with the threat of infection, will depend not only on a host's genetic variability in warmer environments, but also on the frequency of host and pathogen genotypes. We suggest that pathogen‐induced alterations of host thermal performance should be taken into account when assessing the resilience of any population and its potential for adaptation to global change.

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Section: Methodsmentioning

confidence: 99%

Pathogen exposure disrupts an organism's ability to cope with thermal stress

Hector

Sgrò

Hall

2019

Global Change Biology

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“…These five pathogen genotypes vary considerably in virulence (i.e., the reduction of host lifespan) and production of transmission spores (Clerc et al. ; Hall and Mideo ).…”

Section: Methodsmentioning

confidence: 99%

“…After 20 days (at which point all surviving Daphnia will have produced mature transmission spores, Clerc et al. ), all surviving Daphnia (infected and uninfected) were collected, checked for infection under a dissecting microscope, and frozen individually as described above. Spore loads of infected animals were later quantified using an Accuri C6 flow cytometer (BD Biosciences, San Jose, California) following standard procedures as outlined in Gipson and Hall, ().…”

Section: Methodsmentioning

confidence: 99%

Infection in patchy populations: Contrasting pathogen invasion success and dispersal at varying times since host colonization

2019

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Repeated extinction and recolonization events generate a landscape of host populations that vary in their time since colonization. Within this dynamic landscape, pathogens that excel at invading recently colonized host populations are not necessarily those that perform best in host populations at or near their carrying capacity, potentially giving rise to divergent selection for pathogen traits that mediate the invasion process. Rarely, however, has this contention been empirically tested. Using Daphnia magna, we explored how differences in the colonization history of a host population influence the invasion success of different genotypes of the pathogen Pasteuria ramosa. By partitioning the pathogen invasion process into a series of individual steps, we show that each pathogen optimizes invasion differently when encountering host populations that vary in their time since colonization. All pathogen genotypes were more likely to establish successfully in recently colonized host populations, but the production of transmission spores was typically maximized in either the subsequent growth or stationary phase of host colonization. Integrating across the first three pathogen invasion steps (initial establishment, proliferation, and secondary infection) revealed that overall pathogen invasion success (and its variance) was, nonetheless, highest in recently colonized host populations. However, only pathogens that were slow to kill their host were able to maximize host‐facilitated dispersal. This suggests that only a subset of pathogen genotypes—the less virulent and more dispersive—are more likely to encounter newly colonized host populations at the front of a range expansion or in metapopulations with high extinction rates. Our results suggest a fundamental trade‐off for a pathogen between dispersal and virulence, and evidence for higher invasion success in younger host populations, a finding with clear implications for pathogen evolution in spatiotemporally dynamic settings.

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“…), and the relationship between pathogen virulence and transmission (Clerc et al. ; Izhar and Ben‐Ami ), depend on the age of the host, indicating that the optimal infectivity and virulence strategy for a pathogen may be age‐specific. In turn, research has shown that males are more resistant to infection, that mean pathogen fitness is greater within the female host (Duneau et al.…”

Section: Introductionmentioning

confidence: 99%

Interactions between host sex and age of exposure modify the virulence–transmission trade‐off

Gipson

Hall

2018

J of Evolutionary Biology

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The patterns of immunity conferred by host sex or age represent two sources of host heterogeneity that can potentially shape the evolutionary trajectory of disease. With each host sex or age encountered, a pathogen's optimal exploitative strategy may change, leading to considerable variation in expression of pathogen transmission and virulence. To date, these host characteristics have been studied in the context of host fitness alone, overlooking the effects of host sex and age on the fundamental virulence-transmission trade-off faced by pathogens. Here, we explicitly address the interaction of these characteristics and find that host sex and age at exposure to a pathogen affect age-specific patterns of mortality and the balance between pathogen transmission and virulence. When infecting age-structured male and female Daphnia magna with different genotypes of Pasteuria ramosa, we found that infection increased mortality rates across all age classes for females, whereas mortality only increased in the earliest age class for males. Female hosts allowed a variety of trade-offs between transmission and virulence to arise with each age and pathogen genotype. In contrast, this variation was dampened in males, with pathogens exhibiting declines in both virulence and transmission with increasing host age. Our results suggest that differences in exploitation potential of males and females to a pathogen can interact with host age to allow different virulence strategies to coexist, and illustrate the potential for these widespread sources of host heterogeneity to direct the evolution of disease in natural populations.

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Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

Cited by 48 publications

References 42 publications

Pathogen exposure disrupts an organism's ability to cope with thermal stress

Pathogen exposure disrupts an organism's ability to cope with thermal stress

Infection in patchy populations: Contrasting pathogen invasion success and dispersal at varying times since host colonization

Interactions between host sex and age of exposure modify the virulence–transmission trade‐off

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