Bigger is better: changes in body size explain a maternal effect of food on offspring disease resistance

Abstract

Maternal effects triggered by changes in the environment (e.g., nutrition or crowding) can influence the outcome of offspring-parasite interactions, with fitness consequences for the host and parasite. Outside of the classic example of antibody transfer in vertebrates, proximate mechanisms have been little studied, and thus, the adaptive significance of maternal effects on infection is not well resolved. We sought to determine why food-stressed mothers give birth to offspring that show a low rate of infection when the crustacean Daphnia magna is exposed to an orally infective bacterial pathogen. These more-resistant offspring are also larger at birth and feed at a lower rate. Thus, reduced disease resistance could result from slow-feeding offspring ingesting fewer bacterial spores or because their larger size allows for greater immune investment. To distinguish between these theories, we performed an experiment in which we measured body size, feeding rate, and susceptibility, and were able to show that body size is the primary mechanism causing altered susceptibility: Larger Daphnia were less likely to become infected. Contrary to our predictions, there was also a trend that fast-feeding Daphnia were less likely to become infected. Thus, our results explain how a maternal environmental effect can alter offspring disease resistance (though body size), and highlight the potential complexity of relationship between feeding rate and susceptibility in a host that encounters a parasite whilst feeding.

Keywords: host–parasite; life‐history; maternal effects; mechanism; trans‐generational effects.

Figure 1

Maternal food and offspring phenotype. Maternal food (high food—H; low food—L) affects offspring (a) disease resistance (proportion of Daphnia that became infected with Pasteuria ramosa), (b) body size at birth (mean ± SE), and (c) feeding rate (mean ± SE)

Figure 2

Path analysis of routes linking maternal food with the probability of becoming infected following exposure to Pasteuria ramosa. Minimal path model with path coefficients, standard error (in brackets), and p‐values shown next to each significant path

Figure 3

Relationship between body size, feeding rate, and the probability of becoming infected. (a) Feeding rate and body size in the offspring of high‐food (black circles, black line) and low‐food (gray triangles, dashed line) mothers. (b, c) Probability of becoming infected as predicted by a general linear model with body size and feeding rate as explanatory variables