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 .

Social interactions with conspecifics are key to the fitness of most animals and, through the transmission opportunities they provide, are also key to the fitness of their parasites. As a result, research to date has largely focused on the role of host social behavior in imposing selection on parasites, particularly their virulence and transmission phenotypes. However, host social behavior also influences the distribution of parasites among hosts, with implications for their evolution through non-random mating, gene flow, and genetic drift, and thus ability to respond to that selection. Here, we review the paucity of empirical studies on parasites, and draw from empirical studies of free-living organisms and population genetic theory to propose several mechanisms by which host social behavior potentially drives parasite evolution through these less-well studied mechanisms. We focus on the guppy host and Gyrodactylus (Monogenea) ectoparasitic flatworm system and follow a spatially hierarchical outline to highlight that social behavior varies between individuals, and between host populations across the landscape, generating a mosaic of ecological and evolutionary outcomes for their infecting parasites. We argue that the guppy-Gyrodactylus system presents a unique opportunity to address this fundamental knowledge gap in our understanding of the connection between host social behavior and parasite evolution. Individual differences in host social behavior generates fine-scale changes in the spatial distribution of parasite genotypes, shape the size, and diversity of their infecting parasite populations and may generate non-random mating on, and non-random transmission between hosts. While at population and metapopulation level, variation in host social behavior interacts with landscape structure to affect parasite gene flow, effective population size, and genetic drift to alter the coevolutionary potential of local adaptation. Significance statementSocial interactions between animals shape the evolution of the pathogens that infect them. Most research exploring this phenomenon has focused on the selection such interactions impose, but social hosts also shape parasite evolution by determining the ability of their parasites to respond to that selection. Here, we explore how host social behavior drives parasite evolution by shaping non-random mating, gene flow, and genetic drift, from the scale of the individual to the landscape. The relative strength of these evolutionary mechanisms can have striking implications for the evolution of parasite traits such as virulence and alter the evolutionary trajectories of populations across the landscape. We emphasize the importance of studies combining parasite population genetics, host social behavior, and landscape processes to illuminate complex host-parasite coevolutionary dynamics.

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.

Parasites can mediate competition among host species in an ecological community by differentially affecting key parameters that normally give one species a competitive edge. In nature, however, coinfecting parasites that antagonize or facilitate each other, for example by altering cross-protective host immune responses, can modulate host infection outcomes and parasite transmission relative to a single infection. Under what conditions is coinfection likely to interfere with parasite-mediated apparent competition among hosts? To address this question, we created a model of two coinfected host species. Parasites could interact indirectly by affecting host reproduction, or directly by modulating recovery and disease-induced mortality of each host species to a focal infection. We grounded our model with parameters from a classic apparent competition system but allowed for multiple parasite transmission modes and interaction scenarios. Our results suggest that infection-induced mortality has an outsized effect on competition outcomes relative to recovery, but that coinfection-mediated modulation of mortality can produce a range of coexistence or competitive exclusion outcomes. Moreover, while infection prevalence is sensitive to variation in parasite transmission mode, host competitive outcomes are not. Our generalizable model highlights the influence of immunological variation and parasite ecology on community ecology.