Maternal effects in disease resistance: poor maternal environment increases offspring resistance to an insect virus

Abstract

Maternal effects can be adaptive and because of their intrinsic time delays may have important effects on population dynamics. In vertebrates, and increasingly invertebrates, it is well established that offspring defence is in part determined by maternal parasite exposure. It has also been suggested that there may be indirect maternal effects on immunity mediated by other components of the maternal environment, including density and resource availability. Here, we examine the effect maternal resource availability has on the immunity of offspring in an insect-virus system. We use five different maternal resource levels and examine immunity in the offspring both directly, by challenge with a virus, and by measuring a major component of the immune system, across three offspring environments. Both the direct infection assay and the measure of immunocompetence show clearly that offspring from mothers in poor environments are more resistant to parasites. This may result from life-history optimization of mothers in poor environments, or because the poor environment acts as a cue for higher disease risk in the next generation. This emphasizes the importance of maternal effects on disease resistance, mediated through indirect environmental factors that will have important implications to both the ecological and evolutionary dynamics of host-parasite interactions.

Baculovirus-challenge and poor nutrition inflict within-generation fitness costs without triggering transgenerational immune priming

“…Thus, reduced food quantity and/or quality can act as a cue for increased disease risk and lead to heightened investment in disease resistance in the next generation (Ben-Ami et al, 2010;Stjernman and Little, 2011). In the Indian meal moth, P. interpunctella, reduced food quality (replacement of digestible carbohydrate with cellulose) in the parental generation increased the resistance of offspring to a granulovirus (Boots and Roberts, 2012). Similarly, dilution of the standard diet of T. ni with cellulose resulted in offspring that were more resistant to Bt and T. ni SNPV .…”

“…In addition, in a less than optimal parental environment there may be trade-offs between disease resistance and other life history traits. Parents that experience nutritional stress can produce offspring that are more resistant to pathogens (Ben-Ami et al, 2010;Boots and Roberts, 2012;Stjernman and Little, 2011). The complex relationship between nutrient availability and disease resistance has prompted several studies to look at the interaction between parental pathogen exposure and nutrition on offspring immunity and pathogen susceptibility.…”

Transgenerational effects modulate density-dependent prophylactic resistance to viral infection in a lepidopteran pest

“…Indeed, previous models of DDP suggest that the time-delay between changes in population density and the appearance of resistance effects is critical for determining the dynamics of the host-pathogen interaction [26]. The inclusion of transgenerational effects is likely to complicate the dynamical outcome still further [6], with potentially important consequences for assessing the long-term success of pathogens as biocontrol agents, or for predicting the severity of natural disease outbreaks. Competing interests.…”

“…This acquired protection against infection in invertebrates may follow an initial exposure to the same parasite, a different parasite or an immune response elicitor. However, other mechanisms enhancing offspring disease resistance, independent of parental pathogen pre-exposure, have not been widely investigated, although some recent studies have examined the impact of parental nutrition and crowding [5][6][7][8].…”

Transgenerational effect of infection in Plasmodium- infected mosquitoes

“…Factors such as nutritional availability, crowding conditions or the temperature experienced by mothers can affect the ability of their offspring to withstand an infection [1,2]. When such transgenerational maternal effects result in a net increase in the fitness of offspring, they are usually assumed to be adaptive [3].…”