Poor adult nutrition impairs learning and memory in a parasitoid wasp

Abstract

Animals have evolved cognitive abilities whose impairment can incur dramatic fitness costs. While malnutrition is known to impact brain development and cognitive functions in vertebrates, little is known in insects whose small brain appears particularly vulnerable to environmental stressors. Here, we investigated the influence of diet quality on learning and memory in the parasitoid wasp Venturia canescens. Newly emerged adults were exposed for 24 h to either honey, 20% sucrose solution, 10% sucrose solution, or water, before being conditioned in an olfactory associative learning task in which an odor was associated to a host larvae (reward). Honey fed wasps showed 3.5 times higher learning performances and 1.5 times longer memory retention than wasps fed sucrose solutions or water. Poor diets also reduced longevity and fecundity. Our results demonstrate the importance of early adult nutrition for optimal cognitive function in these parasitoid wasps that must quickly develop long-term olfactory memories for searching suitable hosts for their progeny.

Figure 1

Schematic view of the flight tunnel (top view). Individual wasps were introduced in the start chamber and observed choosing between the two odors displayed on filter papers in the decision chambers for 15 min.

Figure 2

Learning. Percentages of correct choices for the conditioned stimulus (CS, orange odor) and no choices (% not responding individuals) for each nutritional condition. In the boxplot, the central line is the median, the edges of the box are the 25th and 75th percentiles, the whiskers extend to the most extreme data points not considered outliers. Outliers are represented by points. Median responses are indicated for each group in the learning performance graph. Generalized Linear Models (GLM) were implemented with the binomial family error and logit link. Different letters above bar plots indicate significant differences between the treatments after Bonferroni correction (P = 0.0125). N = 50 wasps per nutritional condition (200 wasps in total).

Figure 3

Memory retention times. In the boxplot, the central line is the median, the edges of the box are the 25th and 75th percentiles, the whiskers extend to the most extreme data points not considered outliers. Outliers are represented by points. Median memory retention time is indicated for each group in the memory graph. Memory retentions were compared using one way analysis of variance (ANOVA). Different letters indicate significant differences between the treatments after Bonferroni correction (P = 0.0125). N = 50 wasps per nutritional condition and time interval (2400 wasps in total).

Figure 4

Longevity and fecundity. Effect of the nutritional condition (colors) and conditioning (solid or dashed lines) on survival probability (a) and fecundity (b) of female wasps. Survival curves were obtained from Kaplan Meier model (function survfit in R package “survival” (Therneau 2015)). In the boxplot, the central line is the median, the edges of the box are the 25th and 75th percentiles, the whiskers extend to the most extreme data points not considered outliers, outliers are represented by points. Median lifespan is indicated for each group in the fecundity graph. Different letters indicate significant differences between the treatments after Tukey post-hoc.