Abstract
Understanding factors that allow highly virulent parasites to reach high infection prevalence in host populations is important for managing infection risks to human and wildlife health. Multiple transmission routes have been proposed as one mechanism by which virulent pathogens can achieve high prevalence, underscoring the need to investigate this hypothesis through an integrated modelling-empirical framework. Here, we examine a harmful specialist protozoan infecting monarch butterflies that commonly reaches high prevalence (50–100%) in resident populations. We integrate field and modelling work to show that a combination of three empirically-supported transmission routes (vertical, adult transfer and environmental transmission) can produce and sustain high infection prevalence in this system. Although horizontal transmission is necessary for parasite invasion, most new infections post-establishment arise from vertical transmission. Our study predicts that multiple transmission routes, coupled with high parasite virulence, can reduce resident host abundance by up to 50%, suggesting that the protozoan could contribute to declines of North American monarchs.
Highlights
Parasite virulence is often defined as the harm parasites cause their hosts, leading to reduced host fitness [1,2]
Theory predicts that highly virulent pathogens should have more difficulty invading and persisting in host populations owing to the high mortality rate of infected hosts [5,6]
Parasites that reduced host fitness by 50–80% persisted at high prevalence, infected half or more of the host population, and caused declines in host abundance of 50% or more when all three transmission modes operated simultaneously
Summary
Parasite virulence is often defined as the harm parasites cause their hosts, leading to reduced host fitness [1,2]. Prior work [3] showed that monarchs infected by OE as larvae have a lower probability of eclosing and finding mates (θ), produce fewer eggs per day (at per capita rate bI) and experience higher adult mortality (μI; figure 1, equation (2.5)). To examine how model outcomes respond to individual-level impacts of infection, we developed a composite measure of virulence, defined as the proportional reduction in lifetime reproductive success relative to uninfected adults This measure incorporates infection-induced reductions in adult lifespan, egg production, and the probability of eclosion and mating, relative to parameter estimates for uninfected adults (see the electronic supplementary material for derivation). We used R package dESOLVE [38,40] to solve the system of differential equations
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