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  • Publication
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    Inefficient co-feeding transmission of Borrelia afzelii in two common European songbirds
    (2017)
    Heylen, D.
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    Sprong, H.
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    Krawczyk, A.
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    Van Houtte, N.
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    Genne, D.
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    Gomez-Chamorro, A.
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    van Oers, K.
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  • Publication
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    Strain-specific antibodies reduce co-feeding transmission of the Lyme disease pathogen, Borrelia afzelii
    Vector-borne pathogens use a diversity of strategies to evade the vertebrate immune system. Co-feeding transmission is a potential immune evasion strategy because the vector-borne pathogen minimizes the time spent in the vertebrate host. We tested whether the Lyme disease pathogen, Borrelia afzelii, can use co-feeding transmission to escape the acquired immune response in the vertebrate host. We induced a strain-specific, protective antibody response by immunizing mice with one of two variants of OspC (A3 and A10), the highly variable outer surface protein C of Borrelia pathogens. Immunized mice were challenged via tick bite with B.afzelii strains A3 or A10 and infested with larval ticks at days 2 and 34 post-infection to measure co-feeding and systemic transmission respectively. Antibodies against a particular OspC variant significantly reduced co-feeding transmission of the targeted (homologous) strain but not the non-targeted (heterologous) strain. Cross-immunity between OspC antigens had no effect in co-feeding ticks but reduced the spirochaete load twofold in ticks infected via systemic transmission. In summary, OspC-specific antibodies reduced co-feeding transmission of a homologous but not a heterologous strain of B.afzelii. Co-feeding transmission allowed B.afzelii to evade the negative consequences of cross-immunity on the tick spirochaete load.
  • Publication
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    Cross-reactive acquired immunity influences transmission success of the Lyme disease pathogen, Borrelia afzelii
    Cross-reactive acquired immunity in the vertebrate host induces indirect competition between strains of a given pathogen species and is critical for understanding the ecology of mixed infections. In vector-borne diseases, cross-reactive antibodies can reduce pathogen transmission at the vector-to-host and the host-to-vector lifecycle transition. The highly polymorphic, immunodominant, outer surface protein C (OspC) of the tick-borne spirochete bacterium Borrelia afzelii induces a strong antibody response in the vertebrate host. To test how cross-immunity in the vertebrate host influences tick-to-host and host-to-tick transmission, mice were immunized with one of two strain-specific recombinant OspC proteins (A3, A10), challenged via tick bite with one of the two B. afzelii ospC strains (A3, A10), and infested with xenodiagnostic ticks. Immunization with a given rOspC antigen protected mice against homologous strains carrying the same major ospC group allele but provided little or no cross-protection against heterologous strains carrying a different major ospC group allele. There were cross-immunity effects on the tick spirochete load but not on the probability of host-to-tick transmission. The spirochete load in ticks that had fed on mice with cross-immune experience was reduced by a factor of two compared to ticks that had fed on naive control mice. In addition, strain-specific differences in mouse spirochete load, host-to-tick transmission, tick spirochete load, and the OspC-specific IgG response revealed the mechanisms that determine variation in transmission success between strains of B. afzelii. This study shows that cross-immunity in infected vertebrate hosts can reduce pathogen load in the arthropod vector with potential consequences for vector-to-host pathogen transmission. (C) 2015 Elsevier B.V. All rights reserved.
  • Publication
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    Infection dynamics in frog populations with different histories of decline caused by a deadly disease
    (2015-12)
    Sapsford, Sarah J.
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    Alford, Ross A.
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    Schwarzkopf, Lin
    Pathogens can drive host population dynamics. Chytridiomycosis is a fungal disease of amphibians that is caused by the fungus Batrachochytrium dendrobatidis (Bd). This pathogen has caused declines and extinctions in some host species whereas other host species coexist with Bd without suffering declines. In the early 1990s, Bd extirpated populations of the endangered common mistfrog, Litoria rheocola, at high-elevation sites, while populations of the species persisted at low-elevation sites. Today, populations have reappeared at many high-elevation sites where they presently co-exist with the fungus. We conducted a capture-mark-recapture (CMR) study of six populations of L. rheocola over 1 year, at high and low elevations. We used multistate CMR models to determine which factors (Bd infection status, site type, and season) influenced rates of frog survival, recapture, infection, and recovery from infection. We observed Bd-induced mortality of individual frogs, but did not find any significant effect of Bd infection on the survival rate of L. rheocola at the population level. Survival and recapture rates depended on site type and season. Infection rate was highest in winter when temperatures were favourable for pathogen growth, and differed among site types. The recovery rate was high (75.7-85.8 %) across seasons, and did not differ among site types. The coexistence of L. rheocola with Bd suggests that (1) frog populations are becoming resistant to the fungus, (2) Bd may have evolved lower virulence, or (3) current environmental conditions may be inhibiting outbreaks of the fatal disease.
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    The Lyme Disease Pathogen Has No Effect on the Survival of Its Rodent Reservoir Host
    (2015-2-17) ;
    Lachish, Shelly
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    Dolan, Marc C.
    Zoonotic pathogens that cause devastating morbidity and mortality in humans may be relatively harmless in their natural reservoir hosts. The tick-borne bacterium Borrelia burgdorferi causes Lyme disease in humans but few studies have investigated whether this pathogen reduces the fitness of its reservoir hosts under natural conditions. We analyzed four years of capture-mark-recapture (CMR) data on a population of white-footed mice, Peromyscus leucopus, to test whether B. burgdorferi and its tick vector affect the survival of this important reservoir host. We used a multi-state CMR approach to model mouse survival and mouse infection rates as a function of a variety of ecologically relevant explanatory factors. We found no effect of B. burgdorferi infection or tick burden on the survival of P. leucopus. Our estimates of the probability of infection varied by an order of magnitude (0.051 to 0.535) and were consistent with our understanding of Lyme disease in the Northeastern United States. B. burgdorferi establishes a chronic avirulent infection in their rodent reservoir hosts because this pathogen depends on rodent mobility to achieve transmission to its sedentary tick vector. The estimates of B. burgdorferi infection risk will facilitate future theoretical studies on the epidemiology of Lyme disease.
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    Co-feeding transmission in Lyme disease pathogens
    This review examines the phenomenon of co-feeding transmission in tick-borne pathogens. This mode of transmission is critical for the epidemiology of several tick-borne viruses but its importance for Borrelia burgdorferi sensu lato, the causative agents of Lyme borreliosis, is still controversial. The molecular mechanisms and ecological factors that facilitate co-feeding transmission are therefore examined with particular emphasis on Borrelia pathogens. Comparison of climate, tick ecology and experimental infection work suggests that co-feeding transmission is more important in European than North American systems of Lyme borreliosis, which potentially explains why this topic has gained more traction in the former continent than the latter. While new theory shows that co-feeding transmission makes a modest contribution to Borrelia fitness, recent experimental work has revealed new ecological contexts where natural selection might favour co-feeding transmission. In particular, co-feeding transmission might confer a fitness advantage in the Darwinian competition among strains in mixed infections. Future studies should investigate the ecological conditions that favour the evolution of this fascinating mode of transmission in tick-borne pathogens.
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    Genetic variation in transmission success of the Lyme borreliosis pathogen Borrelia afzelii
    The vector-to-host and host-to-vector transmission steps are the two critical events that define the life cycle of any vector-borne pathogen. We expect negative genetic correlations between these two transmission phenotypes, if parasite genotypes specialized at invading the vector are less effective at infecting the vertebrate host and vice versa. We used the tick-borne bacterium Borrelia afzelii, a causative agent of Lyme borreliosis in Europe, to test whether genetic trade-offs exist between tick-to-host, systemic (host-to-tick), and a third mode of co-feeding (tick-to-tick) transmission. We worked with six strains of B. afzelii that were differentiated according to their ospC gene. We compared the three components of transmission among the B. afzelii strains using laboratory rodents as the vertebrate host and a laboratory colony of Ixodes ricinus as the tick vector. We used next generation matrix models to combine these transmission components into a single estimate of the reproductive number (R0) for each B. afzelii strain. We also tested whether these strain-specific estimates of R0 were correlated with the strain-specific frequencies in the field. We found significant genetic variation in the three transmission components among the B. afzelii strains. This is the first study to document genetic variation in co-feeding transmission for any tick-borne pathogen. We found no evidence of trade-offs as the three pairwise correlations of the transmission rates were all positive. The R0 values from our laboratory study explained 45% of the variation in the frequencies of the B. afzelii ospC strains in the field. Our study suggests that laboratory estimates of pathogen fitness can predict the distribution of pathogen strains in nature.