Ecological Context Influences Epidemic Size and Parasite-Driven Evolution

Abstract

The occurrence and magnitude of disease outbreaks can strongly influence host evolution. In particular, when hosts face a resistance-fecundity trade-off, they might evolve increased resistance to infection during larger epidemics but increased susceptibility during smaller ones. We tested this theoretical prediction by using a zooplankton-yeast host-parasite system in which ecological factors determine epidemic size. Lakes with high productivity and low predation pressure had large yeast epidemics; during these outbreaks, hosts became more resistant to infection. However, with low productivity and high predation, epidemics remained small and hosts evolved increased susceptibility. Thus, by modulating disease outbreaks, ecological context (productivity and predation) shaped host evolution during epidemics. Consequently, anthropogenic alteration of productivity and predation might strongly influence both ecological and evolutionary outcomes of disease.

The development of pathogen resistance in Daphnia magna: implications for disease spread in age-structured populations

“…High levels of fish predation could result in populations dominated by juvenile Daphnia, which tend to be more susceptible to infection. Fish predation has been shown to limit the size of epidemics of the yeast parasite Metschnikowia bicuspidata (Duffy et al, 2012); it is thus possible that in addition to the selective culling by fish of parasitised Daphnia or reductions in overall host density (Duffy and Hall, 2008;Duffy et al, 2005), fish predation also alters epidemic size through changes in the age structure, and thus resistance competence, of the population. Of course, predators that select the smallest, and presumably youngest, individuals [like the invertebrate Chaoborus (Riessen and Young, 2005)] will have the opposite effect, resulting in populations dominated by older Daphnia.…”

“…Much work has been carried out on the causes and consequences of variation in age structure (Charlesworth, 1994;De Roos et al, 2003;Sterner, 1998), and the impact of age structure on virulence evolution and epidemic spread (Castillo-Chavez et al, 1989;Duffy et al, 2012). Empirical data on the susceptibility of different age classes could provide insight into how ecological factors that affect age structure could modulate disease resistance and spread.…”

Why Is Living Fast Dangerous? Disentangling the Roles of Resistance and Tolerance of Disease

“…In addition, amphibian species with small-bodied, fast-developing phenotypes were more susceptible to infection by trematodes and, subsequently, more likely to be malformed and die. These and other recent studies (e.g., Nunn et al 2003;Todesco et al 2010;van der Most et al 2011;Duffy et al 2012;Huang et al 2013) suggest that large-bodied, slow-return phenotypes resist pathogen activity. As theoretical models predict that more-resistant phenotypes reduce pathogen transmission and prevalence (e.g., Roy and Kirchner 2000), the evidence suggests that small-bodied, quick-return hosts are less resistant and, thus, have greater potential to contribute to transmission.…”

Climatic and evolutionary drivers of phase shifts in the plague epidemics of colonial India

“…Such traits could also provide a mechanistic basis for counterselection of resistance in our model. Despite considerable attention to the evolutionary impact of pathogens on hosts in ecology, longitudinal studies documenting the inextricably linked dynamics of transmission and pathogenmediated evolutionary selection-and their environmental dependence-have been constrained to a narrow set of systems (22)(23)(24)(25)(26)59). Aided by rich datasets describing epidemiological dynamics, selection, and environmental drivers of transmission, our modeling links Victorian era observations to the longstanding mystery of what caused reductions in epidemic magnitude during the third plague pandemic in India.…”

“…Despite these direct findings regarding expansion of resistance in a host population, in few instances has it been possible to provide insight into the coupled trajectories of transmission, evolutionary dynamics, and their environmental drivers (22). In a model system of the plankton species Daphnia dentifera and its parasite Metschnikowia bicuspidata, environmental factors affecting transmission intermittently alter the intensity of selection for resistance, in turn impacting the size and timing of recurrent epidemics (23)(24)(25). In a rare example from vertebrates, the intensity of seasonal myxomatosis epidemics in Australia predicted year to year variation in the susceptibility of wild rabbits (26) in a broader context of decades-long selection for resistance (12).…”