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Theory often predicts that host populations should evolve greater resistance when parasites become abundant. Furthermore, that evolutionary response could ameliorate declines in host populations during epidemics. Here, we argue for an update: when all host genotypes become sufficiently infected, higher parasite abundance can select for lower resistance because its cost exceeds its benefit. We illustrate such a “resistance is futile” outcome with mathematical and empirical approaches. First, we analyzed an eco-evolutionary model of parasites, hosts, and hosts’ resources. We determined eco-evolutionary outcomes for prevalence, host density, and resistance (mathematically, “transmission rate”) along ecological and trait gradients that alter parasite abundance. With high enough parasite abundance, hosts evolve lower resistance, amplifying infection prevalence and decreasing host density. In support of these results, a higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites in a mesocosm experiment. In two-genotype treatments, zooplankton hosts evolved less resistance under high-nutrient conditions than under low-nutrient conditions. Less resistance, in turn, was associated with higher infection prevalence and lower host density. Finally, in an analysis of naturally occurring epidemics, we found a broad, bimodal distribution of epidemic sizes consistent with the resistance is futile prediction of the eco-evolutionary model. Together, the model and experiment, supplemented by the field pattern, support predictions that drivers of high parasite abundance can lead to the evolution of lower resistance. Hence, under certain conditions, the most fit strategy for individual hosts exacerbates prevalence and depresses host populations. 

Abstract Why do parasites exhibit a wide dynamical range within their hosts? For instance, why does infecting dose either lead to infection or immune clearance? Why do some parasites exhibit boom‐bust, oscillatory dynamics? What maintains parasite diversity, that is coinfectionvsingle infection due to exclusion or priority effects? For insights on parasite dose, dynamics and diversity governing within‐host infection, we turn to niche models. An omnivory food web model (IGP) blueprints one parasite competing with immune cells for host energy (PIE). Similarly, a competition model (keystone predation, KP) mirrors a new coinfection model (2PIE). We then drew analogies between models using feedback loops. The following three points arise: first, like in IGP, parasites oscillate when longer loops through parasites, immune cells and resource regulate parasite growth. Shorter, self‐limitation loops (involving resources and enemies) stabilise those oscillations. Second, IGP can produce priority effects that resemble immune clearance. But, despite comparable loop structure, PIE cannot due to constraints imposed by production of immune cells. Third, despite somewhat different loop structure, KP and 2PIE share apparent and resource competition mechanisms that produce coexistence (coinfection) or priority effects of prey or parasites. Together, this mechanistic niche framework for within‐host dynamics offers new perspective to improve individual health. 

Genetic variation in parasites has important consequences for host-parasite interactions. Prior studies of the ecologically important parasite Metschnikowia bicuspidata have suggested low genetic variation in the species. Here, we collected M. bicuspidata from two host species (Daphnia dentifera and Ceriodaphnia dubia) and two regions (Michigan and Indiana, USA). Within a lake, outbreaks tended to occur in one host species but not the other. Using microsatellite markers, we identified six parasite genotypes grouped within three distinct clades, one of which was rare. Of the two main clades, one was generally associated with D. dentifera, with lakes in both regions containing a single genotype. The other M. bicuspidata clade was mainly associated with C. dubia, with a different genotype dominating in each region. Despite these associations, both D. dentifera- and C. dubia-associated genotypes were found infecting both hosts in lakes. However, in lab experiments, the D. dentifera-associated genotype infected both D. dentifera and C. dubia, but the C. dubia-associated genotype, which had spores that were approximately 30% smaller, did not infect D. dentifera. We hypothesize that variation in spore size might help explain patterns of cross-species transmission. Future studies exploring the causes and consequences of variation in spore size may help explain patterns of infection and the maintenance of genotypic diversity in this ecologically important system. 

Abstract The healthy herds hypothesis proposes that predators can reduce parasite prevalence and thereby increase the density of their prey. However, evidence for such predator‐driven reductions in the prevalence of prey remains mixed. Furthermore, even less evidence supports increases in prey density during epidemics. Here, we used a planktonic predator–prey–parasite system to experimentally test the healthy herds hypothesis. We manipulated density of a predator (the phantom midge,Chaoborus punctipennis) and parasitism (the virulent fungusMetschnikowia bicuspidata) in experimental assemblages. Because we know natural populations of the prey (Daphnia dentifera) vary in susceptibility to both predator and parasite, we stocked experimental populations with nine genotypes spanning a broad range of susceptibility to both enemies. Predation significantly reduced infection prevalence, eliminating infection at the highest predation level. However, lower parasitism did not increase densities of prey; instead, prey density decreased substantially at the highest predation levels (a major density cost of healthy herds predation). This density result was predicted by a model parameterized for this system. The model specifies three conditions for predation to increase prey density during epidemics: (i) predators selectively feed on infected prey, (ii) consumed infected prey release fewer infectious propagules than unconsumed prey, and (iii) sufficiently low infection prevalence. While the system satisfied the first two conditions, prevalence remained too high to see an increase in prey density with predation. Low prey densities caused by high predation drove increases in algal resources of the prey, fueling greater reproduction, indicating that consumer–resource interactions can complicate predator–prey–parasite dynamics. Overall, in our experiment, predation reduced the prevalence of a virulent parasite but, at the highest levels, also reduced prey density. Hence, while healthy herds predation is possible under some conditions, our empirical results make it clear that the manipulation of predators to reduce parasite prevalence may harm prey density. 

Abstract Parasite transmission is thought to depend on both parasite exposure and host susceptibility to infection; however, the relative contribution of these two factors to epidemics remains unclear. We used interactions between an aquatic host and its fungal parasite to evaluate how parasite exposure and host susceptibility interact to drive epidemics. In six lakes, we tracked the following factors from pre‐epidemic to epidemic emergence: (1) parasite exposure (measured observationally as fungal spores attacking wild‐caught hosts), (2) host susceptibility (measured experimentally as the number of fungal spores required to produce terminal infection), (3) host susceptibility traits (barrier resistance and internal clearance, both quantified with experimental assays), and (4) parasite prevalence (measured observationally from wild‐caught hosts). Tracking these factors over 6 months and in almost 7,000 wild‐caught hosts provided key information on the drivers of epidemics. We found that epidemics depended critically on the interaction of exposure and susceptibility; epidemics only emerged when a host population’s level of exposure exceeded its individuals’ capacity for recovery. Additionally, we found that host internal clearance traits (the hemocyte response) were critical in regulating epidemics. Our study provides an empirical demonstration of how parasite exposure and host susceptibility interact to inhibit or drive disease in natural systems and demonstrates that epidemics can be delayed by asynchronicity in the two processes. Finally, our results highlight how individual host traits can scale up to influence broad epidemiological patterns.