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

Abstract

Immunity in vertebrates is well established to develop with time, but the ontogeny of defence in invertebrates is markedly less studied. Yet, age-specific capacity for defence against pathogens, coupled with age structure in populations, has widespread implications for disease spread. Thus, we sought to determine the susceptibility of hosts of different ages in an experimental invertebrate host-pathogen system. In a series of experiments, we show that the ability of Daphnia magna to resist its natural bacterial pathogen Pasteuria ramosa changes with host age. Clonal differences make it difficult to draw general conclusions, but the majority of observations indicate that resistance increases early in the life of D. magna, consistent with the idea that the defence system develops with time. Immediately following this, at about the time when a daphnid would be most heavily investing in reproduction, resistance tends to decline. Because many ecological factors influence the age structure of Daphnia populations, our results highlight a broad mechanism by which ecological context can affect disease epidemiology. We also show that a previously observed protective effect of restricted maternal food persists throughout the entire juvenile period, and that the protective effect of prior treatment with a small dose of the pathogen ('priming') persists for 7 days, observations that reinforce the idea that immunity in D. magna can change over time. Together, our experiments lead us to conclude that invertebrate defence capabilities have an ontogeny that merits consideration with respect to both their immune systems and the epidemic spread of infection.

Keywords: Age; Daphnia; Epidemiology; Immunity; Invertebrate; Ontogeny.

Fig. 1.

The development of resistance in Daphnia magna. The mean predicted proportion of D. magna infected following a 4 h exposure to the pathogen Pasteuria ramosa at one of eight ages (in days). Each data point represents the mean proportion of infected Daphnia across both clones, as predicted by the generalised linear model. Error bars show the variation between clones, and are the standard errors of the predicted values for each clone. Note that 30 and 40 day old Daphnia were exposed on the same day as the 0 and 10 day olds.

Fig. 2.

Maternal effects on the early development of resistance. The mean predicted proportion of D. magna infected following exposure to P. ramosa at one of four ages (in days) early in life. The mothers of these Daphnia were raised under either high food (HF) or low food (LF). Each data point represents the mean proportion of infected Daphnia across three clones, as predicted by the generalised linear model. Error bars show the variation between clones, and are the standard errors of the predicted values for each clone.

Fig. 3.

Priming and the development of resistance. The mean predicted proportion of D. magna infected after exposure to P. ramosa at three different time points following a primary (and non-infective) exposure to the pathogen (filled circles) or a control exposure (open circles). Each data point represents the mean proportion of infected Daphnia across four clones, as predicted by the generalised linear model. Error bars show the variation between clones, and are the standard errors of the predicted values for each clone.

Fig. 4.

The development of resistance with longer exposure times. The proportion of D. magna infected following exposure to the pathogen P. ramosa at one of eight ages (in days). Each exposure period lasted 5 days, and thus the day shown is the first day of a relatively long exposure period.