Disentangling the influence of parasite genotype, host genotype and maternal environment on different stages of bacterial infection in Daphnia magna

Abstract

Individuals naturally vary in the severity of infectious disease when exposed to a parasite. Dissecting this variation into genetic and environmental components can reveal whether or not this variation depends on the host genotype, parasite genotype or a range of environmental conditions. Complicating this task, however, is that the symptoms of disease result from the combined effect of a series of events, from the initial encounter between a host and parasite, through to the activation of the host immune system and the exploitation of host resources. Here, we use the crustacean Daphnia magna and its parasite Pasteuria ramosa to show how disentangling genetic and environmental factors at different stages of infection improves our understanding of the processes shaping infectious disease. Using compatible host-parasite combinations, we experimentally exclude variation in the ability of a parasite to penetrate the host, from measures of parasite clearance, the reduction in host fecundity and the proliferation of the parasite. We show how parasite resistance consists of two components that vary in environmental sensitivity, how the maternal environment influences all measured aspects of the within-host infection process and how host-parasite interactions following the penetration of the parasite into the host have a distinct temporal component.

Expression of parasite genetic variation changes over the course of infection: implications of within-host dynamics for the evolution of virulence

“…Recent work has suggested that genetic variation in disease characteristics can vary considerably over the course of infection, potentially influencing the evolution of the parasite [9,11,18]. Here, we quantified parasite genetic variation for three key disease traits over the duration of an entire infection process.…”

“…the degree of differences among parasite genotypes) of virulence and transmission changes with the age of the infection, raising the question whether such within-host dynamics matter for the evolution of the parasite and thus for disease traits? Ultimately, the consequences of any within-host patterns for evolutionary dynamics depend on a direct link to parasite transmission success [9,11,18]. A lack of variability (and evolutionary potential) early in the infection process would be irrelevant if all infected animals were able to progress through to the end of the infection process, when the parasite induces host death.…”

“…Offspring were counted at each changing event (twice a week), with survival monitored daily and any dead animals frozen for later spore counting. At 18 rspb.royalsocietypublishing.org Proc. R. Soc.…”

“…For other unmeasured host and parasite combinations, however, the relative importance of castration onset and efficiency will likely vary. A number of studies have documented differences between host and parasite genotypes in many characteristics of the early phase of infection, including time until initial castration, early fecundity and initial spore growth [18,21,[36][37][38]. By using only one host genotype, we inevitably excluded an important component of variability, including the potential for host-by-pathogen genetic interactions.…”

Genetic architecture of resistance in Daphnia hosts against two species of host-specific parasites

“…Steps of the infection process P. ramosa's infection process can be subdivided into a number of steps: encounter, spore activation, attachment, penetration of the host cuticle and within-host steps (Duneau et al, 2011;Hall and Ebert, 2012). The host's interference with any of these steps could contribute to host resistance.…”