Gene-environment interplay in Drosophila melanogaster: chronic food deprivation in early life affects adult exploratory and fitness traits

Abstract

Early life adversity has known impacts on adult health and behavior, yet little is known about the gene-environment interactions (GEIs) that underlie these consequences. We used the fruit fly Drosophila melanogaster to show that chronic early nutritional adversity interacts with rover and sitter allelic variants of foraging (for) to affect adult exploratory behavior, a phenotype that is critical for foraging, and reproductive fitness. Chronic nutritional adversity during adulthood did not affect rover or sitter adult exploratory behavior; however, early nutritional adversity in the larval period increased sitter but not rover adult exploratory behavior. Increasing for gene expression in the mushroom bodies, an important center of integration in the fly brain, changed the amount of exploratory behavior exhibited by sitter adults when they did not experience early nutritional adversity but had no effect in sitters that experienced early nutritional adversity. Manipulation of the larval nutritional environment also affected adult reproductive output of sitters but not rovers, indicating GEIs on fitness itself. The natural for variants are an excellent model to examine how GEIs underlie the biological embedding of early experience.

Fig. 1.

Behavior of female sitters in the open field was more sensitive to larval nutritional adversity than the behavior of female rovers. (A) Darting exploration of sitters was significantly higher when reared in early nutritional adversity than when reared in standard conditions (post hoc ANOVA, P < 0.001), but rover behavior was not significantly different between food treatments (P = 0.11). Darting exploration is the first component of a principal components analysis of distance, inner zone frequency per second of movement, and mean MSDR during movement periods. (B) Both sitters (P < 0.001) and rovers (P = 0.002) walked shorter distances when reared in early nutritional adversity than when reared in standard conditions. (C) Number of crossings into the inner zone of the open field, per second of movement, of sitters was significantly higher when reared in early nutritional adversity than when reared in standard conditions (P < 0.001), but rover behavior was not significantly different between food treatments (P = 0.58). (D) MSDR of sitters was significantly higher when reared in early nutritional adversity than when reared in standard conditions (P = 0.016), but rover behavior was not significantly different between food treatments (P = 0.89). Lines above bars indicate a significant difference between groups at the terminus of the line. Error bars represent SEM.

Fig. 2.

Increased for expression in MBs, using the UAS-Gal4 system in a sitter genetic background, recovered rover exploratory behavior in female flies. All three drivers are expressed in the α- and β-lobes, 30Y and 201Y are expressed in the γ-lobes, and 30Y is also expressed in the neurons that project to the α′- and β′-lobes (22). Black bars represent the UAS-Gal4 experimental crosses, white bars represent the Gal4 control crosses, and gray bars represent the UAS control crosses. (A) Darting exploration was greater in all three MB drivers. (B) Distance moved was significantly lower in the 30Y-Gal4 and 201Y-Gal4 driver lines and marginally lower in the c739-Gal4 driver line. (C) Inner zone exploration was significantly higher in the 30Y-Gal4 and 201Y-Gal4 driver lines and marginally higher in the c739-Gal4 driver line. (D) MSDR was significantly higher in all three MB driver lines. The symbols above the bars show the significance of a planned contrast between a given UAS × Gal4 line and the two corresponding controls (Gal4 × w¹;for^s and w¹;for^s × UAS) in the ANOVA, corrected for multiple comparisons by the Holm–Bonferroni method. Error bars represent SEM. ***P < 0.001; **P < 0.01; *P < 0.05; °P < 0.10.

Fig. 3.

Female sitters reared in nutritional adversity as larvae laid fewer eggs than sitters reared in standard conditions (post hoc ANOVA, P = 0.015), but no effect of nutritional environment was detected in rovers (P = 0.768). The line above the bars indicates a significant difference between groups at the terminus of the line. Error bars represent SEM.