Humans have contributed to the increased frequency and severity of emerging infectious diseases, which pose a significant threat to wild and domestic species, as well as human health. This review examines major pathways by which humans influence parasitism by altering (co)evolutionary interactions between hosts and parasites on ecological timescales. There is still much to learn about these interactions, but a few well-studied cases show that humans influence disease emergence every step of the way. Human actions significantly increase dispersal of host, parasite and vector species, enabling greater frequency of infection in naive host populations and host switches. Very dense host populations resulting from urbanization and agriculture can drive the evolution of more virulent parasites and, in some cases, more resistant host populations. Human activities that reduce host genetic diversity or impose abiotic stress can impair the ability of hosts to adapt to disease threats. Further, evolutionary responses of hosts and parasites can thwart disease management and biocontrol efforts. Finally, in rare cases, humans influence evolution by eradicating an infectious disease. If we hope to fully understand the factors driving disease emergence and potentially control these epidemics we must consider the widespread influence of humans on host and parasite evolutionary trajectories. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

In tri-trophic systems, herbivores may benefit from their host plants in fighting parasitic infections. Plants can provide parasite resistance in two contrasting ways: either directly, by interfering with the parasite, or indirectly, by increasing herbivore immunity or health. In monarch butterflies, the larval diet of milkweed strongly influences the fitness of a common protozoan parasite. Toxic secondary plant chemicals known as cardenolides correlate strongly with parasite resistance of the host, with greater cardenolide concentrations in the larval diet leading to lower parasite growth. However, milkweed cardenolides may covary with other indices of plant quality including nutrients, and a direct experimental link between cardenolides and parasite performance has not been established. To determine if the anti-parasitic activity of milkweeds is indeed due to secondary chemicals, as opposed to nutrition, we supplemented the diet of infected and uninfected monarch larvae with milkweed latex, which contains cardenolides but no nutrients. Across three experiments, increased dietary cardenolide concentrations reduced parasite growth in infected monarchs, which consequently had longer lifespans. However, uninfected monarchs showed no differences in lifespan across treatments, confirming that cardenolide-containing latex does not increase general health. Our results suggest that cardenolides are a driving force behind plant-derived resistance in this system.

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Host-parasite interactions are subject to strong trait-mediated indirect effects from other species. However, it remains unexplored whether such indirect effects may occur across soil boundaries and connect spatially isolated organisms. Here, we demonstrate that, by changing plant (milkweed Asclepias sp.) traits, arbuscular mycorrhizal fungi (AMF) significantly affect interactions between a herbivore (the monarch butterfly Danaus plexippus) and its protozoan parasite (Ophryocystis elektroscirrha), which represents an interaction across four biological kingdoms. In our experiment, AMF affected parasite virulence, host resistance and host tolerance to the parasite. These effects were dependent on both the density of AMF and the identity of milkweed species: AMF indirectly increased disease in monarchs reared on some species, while alleviating disease in monarchs reared on other species. The speciesspecificity was driven largely by the effects of AMF on both plant primary ( phosphorus) and secondary (cardenolides; toxins in milkweeds) traits. Our study demonstrates that trait-mediated indirect effects in disease ecology are extensive, such that below-ground interactions between AMF and plant roots can alter host-parasite interactions above ground. In general, soil biota may play an underappreciated role in the ecology of many terrestrial host-parasite systems.

Many studies have used host-parasite systems to study local adaptation, but few of these studies have found unequivocal evidence for adaptation. One potential reason is that most studies have focused on limited measures of host and parasite fitness that are generally assumed to be under negative frequency-dependent selection. We have used reciprocal cross-infection experiments to test for local adaptation in Hawaiian, south Floridian, and eastern North American populations of monarch butterflies and their protozoan parasites. Sympatric host-parasite combinations did not result in greater host or parasite fitness, as would be expected under coevolutionary dynamics driven by negative frequency-dependent selection. Instead, we found that Hawaiian hosts were more resistant and carried more infective and virulent parasites, which is consistent with theoretical predictions for virulence evolution and coevolutionary arms race dynamics. We also found that Hawaiian hosts were more tolerant, particularly of Hawaiian parasites, indicating that increased resistance does not preclude increased tolerance within a population and that hosts may be more tolerant of local parasites. We did not find a similar pattern in the south Floridian or eastern populations, possibly because host-parasite adaptation occurs within the context of a greater ecological community.

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A major challenge in evolutionary biology is explaining variation in reproductive strategies-especially why so many organisms re-

Symbiosis is increasingly recognized as a dynamic relationship, with the net outcome falling along a continuum from mutualism to parasitism. A key example of this comes from a recently discovered microsporidian symbiont ofDaphnia, the net impact of which was found to vary from negative to positive. We investigated the taxonomic position of this microsporidian and the morphology of infected hosts, as well as the virulence, ecology and host range of the symbiont; we also provide information about its culturing methods. The genetic data indicates that the microsporidian symbiont belongs toOrdospora pajunii, a newly described microsporidian parasite ofDaphnia. We show thatO. pajuniiinfection damages the gut, causing infected epithelial cells to lose microvilli and then rupture. The prevalence of this microsporidian can be high (up to 100% in the lab and 77% of adults in the field). Its overall virulence seems low in most cases, but some genotypes suffer reduced survival and reproduction. Susceptibility and virulence are strongly host-genotype dependent. We found that North AmericanO. pajuniiare able to infect multipleDaphniaspecies, including the European speciesD. longispina, as well as the genusCeriodaphnia. We propose theDaphnia-O. pajuniisymbiosis as a valuable system for studying the mechanisms of context-dependent shifts between mutualism and parasitism, as well as for understanding how symbionts might alter host interactions with resources.