Parasites exploit hosts to replicate and transmit, but overexploitation kills host and parasite (1): predators may shift this cost-benefit balance by consuming hosts (2-4) or changing host behavior, but the strength of these effects remains unclear. Modeling both, we find a primary, strong effect: hosts group to defend against predators (5), increasing parasite transmission, thus multiple infections, and therefore favoring more exploitative, virulent, parasites (6). Indeed, among 18 Trinidadian Gyrodactyus spp. parasite lines, those collected from high predation guppy populations were more virulent in common garden than those from low .

Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite: parasite virulence evolves to balance these costs and benefits. Predators can in theory shift this balance by consuming hosts. However, the non-consumptive effects of predators may be as important as their consumptive effects. Here, we use an eco-coevolutionary model to show that predators select for host grouping, a common anti-predator, defensive social behaviour. Host grouping simultaneously increases parasite transmission, thus within-host parasite competition, and therefore favours more exploitative, virulent, parasites. When parametrized with data from the guppy-Gyrodactylus spp. system, including our experimentally demonstrated trade-off between virulence and transmission, our model accurately predicted the common garden-assayed virulence of 18 parasite lines collected from four Trinidadian guppy populations under different predation regimes. The quantitative match between theory and data lends credence to the model insight that the non-consumptive, social behaviour pathway is entirely responsible for the observed increase in virulence with predation pressure. Our results indicate that parasites play an important, underappreciated role in guppy evolutionary ecology. Moreover, group living is a common anti-predator defence and our general model accommodates host-parasite interactions across taxa: its insight into the interactions among predation, sociality, and virulence evolution may apply broadly. Our results additionally suggest that social distancing, by reducing host-host contact, can select for less virulent parasites and pathogens.

What determines how much resistance hosts evolve? One might intuit that hosts evolve higher resistance when parasites are more abundant. However, the opposite pattern can arise due to costs of resistance. Here we illustrate with mathematical, experimental, and field approaches how ecological context can increase parasite abundance and select for lower resistance. "Resistance is futile" when all host genotypes become sufficiently infected. To make this argument, we first analyzed an eco-evolutionary model of parasites, hosts, and resources of hosts. We determined eco-evolutionary outcomes for resistance (mathematically, transmission rate) and densities along gradients that drive epidemic size. When epidemic drivers are high, hosts evolve lower resistance, amplifying epidemics and decreasing host density. Experimental mesocosms qualitatively agreed. In the experiment, higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites. Evolving zooplankton hosts were less resistant at high nutrients than at low. Less resistance, in turn, was associated with higher infection prevalence and lower host density. We also analyzed the size of naturally occurring epidemics, finding a broad, bimodal distribution of epidemic sizes consistent with the eco-evolutionary model. Together, our three approaches supported predictions that high epidemic drivers lead to evolution of lower resistance which drives higher prevalence and lower host density.

Most evolutionary theory predicts that, during epidemics, hosts will evolve higher resistance to parasites that kill them. Here, we provide an alternative to that typical expectation, with an explanation centered on resource feedbacks. When resistance is costly, hosts evolve decreasing resistance without parasites, as expected. But with parasites, hosts can evolve lower resistance than they would in the absence of parasites. This outcome arises in an eco-evolutionary model when four conditions are met: first, resistance has a fecundity cost (here, via decreased foraging/exposure rate); second, resources increase during epidemics via trophic cascades; third, increased resources magnify the benefit of maintaining a fast foraging rate, thereby magnifying the cost of evolving a slower foraging/exposure rate (i.e., resistance); fourth, that amplification of the cost outweighs the benefit of resistance. When these conditions are met, hosts evolve lower resistance than without parasites. This phenomenon was previously observed in a mesocosm experiment with fungal parasites, zooplankton hosts, and algal resources. Re-analyzing this experiment produced evidence for our model’s mechanism. Thus, both model and experiment indicate that, via resource feedbacks, parasites can counterintuitively select against resistance.

1. Parasites kill hosts but also can indirectly increase the abundance of their resources. Given this resource feedback, how much will parasites decrease host density? Can they increase host density? Seeking answers, we integrate trait measurements, a resource-host-parasite model and experimental epidemics with plankton. This combination reveals how parasites may decrease or increase host density. This spectrum of outcomes reflects tension between parasitedriven mortality (a density-mediated effect) and foraging depression upon contact with parasite propagules (a trait-mediated one).2. In the model, mortality rises when higher susceptibility to infection increases infection prevalence. These large epidemics release resources while suppressing hosts (creating a trophic cascade). In contrast, when hosts are less susceptible and parasites depress host foraging, a resource feedback can elevate host density during epidemics (creating a hydra effect), particularly at higher carrying capacity of resources. This combination creates the hydra effect because it elevates primary production relative to per-host consumption of resources (two key determinants of host density).3. We test these predictions qualitatively with trait measurements and a mesocosm experiment. Clonal lines of zooplankton hosts differed in their foraging depression and susceptibility. Then, with these different host genotypes, we created epidemics in mesocosms supplied with either low or high nutrients (to manipulate carrying capacity). Hydra effects and trophic cascades both arose and in the trait-nutrient combinations predicted by the model. 4. Hence, we show how tension between trait-and density-mediated effects of parasites can govern the fate of host density during epidemics-from trophic cascades to hydra effects.