Dopamine mediates the pea aphid wing plasticity

Abstract

Many organisms exhibit phenotypic plasticity, in which developmental processes result in different phenotypes depending on their environmental context. Here we focus on the molecular mechanisms underlying that environmental response. Pea aphids (Acyrthosiphon pisum) exhibit a wing dimorphism, in which pea aphid mothers produce winged or wingless daughters when exposed to a crowded or low-density environment, respectively. We investigated the role of dopamine in mediating this wing plasticity, motivated by a previous study that found higher dopamine titres in wingless- versus winged-producing aphid mothers. In this study, we found that manipulating dopamine levels in aphid mothers affected the numbers of winged offspring they produced. Specifically, asexual female adults injected with a dopamine agonist produced a lower percentage of winged offspring, while asexual females injected with a dopamine antagonist produced a higher percentage of winged offspring, matching expectations based on the titre difference. We also found that genes involved in dopamine synthesis, degradation and signalling were not differentially expressed between wingless- and winged-producing aphids. This result indicates that titre regulation possibly happens in a non-transcriptional manner or that sampling of additional timepoints or tissues is necessary. Overall, our work emphasizes that dopamine is an important component of how organisms process information about their environments.

Keywords: dopamine; pea aphid; phenotypic plasticity; wing dimorphism.

Figure 1.

Manipulating dopamine levels in pea aphid mothers changes the percentage of winged daughters they produce. The y-axis shows the winged percentage of offspring from injected aphid mothers. Breaks on the x-axis show two different experiment rounds (1 and 2). Each data point represents one biological replicate (comprising all the offspring from three aphid mothers produced within the first 24 h after injection; we only retained replicates with six or more offspring), with the total number of biological replicates shown for each treatment (n). The size of the point gives a relative indication of the number of offspring that contributed to that replicate. Triangles represent statistical outliers for the boxplot. Asterisks show significance level (Wilcoxon rank-sum tests; *adjusted p-value ≤ 0.05, ** ≤ 0.01, *** ≤ 0.001).

Figure 2.

Dopamine-related gene expression levels generally do not differ in aphid mothers experiencing crowded versus solitary treatments. The genes are broken up into the categories of (a) dopamine and dopamine/ecdysteroid receptors, (b) dopamine release or transport, or (c) dopamine biogenesis. The y-axis shows expression level in normalized read counts, with each gene having a different axis. The x-axis shows the five different aphid lines. Crowded (wing-producing) or solitary (wingless-producing) treatment means aphids were kept in those conditions for 12 or 16 h (see Methods). Each point represents a biological replicate. Lines 319, C74, 200 and 218 each have three biological replicates per treatment. Line ROC1 has four biological replicates per treatment. Gene names are as in electronic supplementary material, table S2. *Adjusted p-value ≤ 0.05, ** ≤ 0.01, *** ≤ 0.001).