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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. 

Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite. Predators may shift this cost–benefit balance by consuming infected hosts or changing host behaviour, but the strength of these effects remains unclear. Here we use field and lab data on Trinidadian guppies and their Gyrodactylus spp. parasites to show how differential predation pressure influences parasite virulence and transmission. We use an experimentally demonstrated virulence–transmission trade-off to parametrize a mathematical model in which host shoaling (as a means of anti-predator defence), increases contact rates and selects for higher virulence. Then we validate model predictions by collecting parasites from wild, Trinidadian populations; parasites from high-predation populations were more virulent in common gardens than those from low-predation populations. Broadly, our results indicate that reduced social contact selects against parasite virulence.