Epidemiological, Evolutionary, and Coevolutionary Implications of Context-Dependent Parasitism

Abstract

Victims of infection are expected to suffer increasingly as parasite population growth increases. Yet, under some conditions, faster growing parasites do not appear to cause more damage and infections can be quite tolerable. We studied these conditions by assessing how the relationship between parasite population growth and host health is sensitive to environmental variation. In experimental infections of the crustacean Daphnia magna and its bacterial parasite Pasteuria ramosa we show how easily an interaction can shift from a severe interaction, i.e. when host fitness declines substantially with each unit of parasite growth, to a tolerable relationship by changing only simple environmental variables: temperature and food availability. We explored the evolutionary and epidemiological implications of such a shift by modelling pathogen evolution and disease spread under different levels of infection severity, and find that environmental shifts that promote tolerance ultimately result in populations harbouring more parasitized individuals. We also find that the opportunity for selection, as indicated by the variance around traits, varied considerably with the environmental treatment. Thus our results suggest two mechanisms that could underlie co-evolutionary hot-and coldspots: spatial variation in tolerance and spatial variation in the opportunity for selection.

Host resistance and tolerance of parasitic gut worms depend on resource availability

“…Other studies have also found that higher resource availability can increase host tolerance of parasites (Sternberg et al 2012; Howick and Lazzaro 2014). For example, Vale et al (2011) found that on a high resource diet, competition for food resources between Daphnia hosts and their bacterial parasites was reduced allowing for increased host tolerance. Additionally, baseline metabolic rate of hosts can increase in responses to parasitism (Connors and Nickol 1991; Careau et al 2010) and in turn, hosts may increase food intake to compensate for energy lost to parasitism (i.e.…”

“…However, resources may affect reproductive success or biomass (i.e. measure of virulence for macroparasites) of parasites and thus over time, parasite numbers may increase as host tolerance increases in the population (Vale et al 2011). We did not quantify fecundity or biomass of worms in frogs under varying resource conditions but this question could be addressed in the future.…”

“…Higher resource availability can increase microparasite virulence while in a host so hosts might invest more in resistance mechanisms to reduce parasite fitness. However, when the cost of parasitism is less than the cost of resistance, hosts may alternatively invest in tolerance mechanisms (Vale et al 2011). Higher resource availability can increase the virulence of macroparasites by increasing their biomass but may not increase virulence to the extent that resources affect microparasite virulence because macroparasite offspring are typically released from a host to infect a different host.…”

“…For many vertebrate host species, higher food availability decreases abundance of parasites that consume host tissue (Cressler et al 2014), which suggests that these hosts are investing extra resources to resist their parasites and associated tissue damage. In contrast, increased food availability for other animal hosts, such as Daphnia , favors increased tolerance of parasites with whom they share food with, likely because more food for both the host and parasite reduces competition (Vale et al 2011). The type of resource the parasites are consuming and/or damaging can also depend on the stage of the infection.…”

Diet quality determines interspecific parasite interactions in host populations

“…2010; Vale et al. 2011). Evidence for the relevance of these factors, with respect to single species infections, is amply present in a number of different systems: bacteria–phage interactions (Forde et al.…”