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.

Daphnia magna microRNAs respond to nutritional stress and ageing but are not transgenerational

“…The crustacean Daphnia magna exhibits clear maternal effects on size at birth and later performance traits (Ebert, ; Garbutt & Little, ; Lampert, ; Stjernman & Little, ; Tollrian, ): offspring of older mothers or those from calorie‐restricted mothers are larger and show enhanced resistance to pathogens than offspring of young or well‐fed mothers (Clark, Garbutt, McNally, & Little, ; Garbutt & Little, ). Almost half of offspring phenotypic variation (48%) in Daphnia pulex is due to maternal age (Plaistow, Shirley, Collin, Cornell, & Harney, ).…”

“…Our aim was to dissect maternal effects and microRNA responses to environmental variation in the cyclically parthenogenetic crustacean Daphnia magna . We use D. magna for this purpose because it has clear maternal effect phenotypes in response to variation in food nutrition and age (Clark et al., ; Garbutt & Little, ). These strong maternal effects appear to be adaptive, and in the absence of genetic variation, we hypothesize they are controlled by a mixture of provisioning and epigenetic modifications, including miRNAs.…”

Disease spread in age structured populations with maternal age effects

“…; Lorenz & Koella ; Stjernman & Little ; Tidbury et al . ; Boots & Roberts ; Garbutt & Little ). This suggests variation in phenotypic traits, as a response to the maternal environment, can drive population and epidemiological dynamics (Beckerman et al .…”

“…Generally, maternal effects have been shown to affect population dynamics and demography through alterations in offspring reproduction, maturation and growth rate (Gaillard et al 2003;Benton et al 2005;Beamonte-Barrientos et al 2010), and maternal effects have been shown to alter population robustness in the face of ecological challenges (R€ as€ anen & Kruuk 2007;Kuijper & Hoyle 2015). The maternal condition, for example nutrition availability or disease status, is increasingly recognised to affect offspring susceptibility to infection (Huang & Song 1999;Little et al 2003;Rahman et al 2004;Mitchell & Read 2005;Gasparini et al 2007;Lorenz & Koella 2011;Stjernman & Little 2011;Tidbury et al 2011;Boots & Roberts 2012;Garbutt & Little 2017). This suggests variation in phenotypic traits, as a response to the maternal environment, can drive population and epidemiological dynamics (Beckerman et al 2002;Mitchell & Read 2005;Garbutt et al 2014b).…”

Testing hypotheses for maternal effects inDaphnia magna

“…Similar observations have been made in our study species, the crustacean Daphnia magna, where we have observed that increasing maternal age is linked to increasing size at birth, enhanced parasite resistance and changes in reproduction (Clark et al ., ). Variation in maternal nutrition in D. magna appears to produce similar phenotypes, as the offspring of dietary restricted mothers produce relatively large, parasite resistant offspring (Garbutt & Little, ). These increases in body size in offspring from dietary restricted mothers may be adaptive if these mothers can expect their offspring to be born into a low food/high competition environment, and assuming that large offspring have an advantage in this circumstance.…”