Hormonal modulation of reproduction and fertility signaling in polistine wasps

Abstract

In social insects, it has been suggested that reproduction and the production of particular fertility-linked cuticular hydrocarbons (CHC) may be under shared juvenile hormone (JH) control, and this could have been key in predisposing such cues to later evolve into full-fledged queen pheromone signals. However, to date, only few studies have experimentally tested this "hormonal pleiotropy" hypothesis. Here, we formally test this hypothesis using data from four species of Polistine wasps, Polistes dominula, Polistes satan, Mischocyttarus metathoracicus, and Mischocyttarus cassununga, and experimental treatments with JH using the JH analogue methoprene and the anti-JH precocene. In line with reproduction being under JH control, our results show that across these four species, precocene significantly decreased ovary development when compared with both the acetone solvent-only control and the methoprene treatment. Consistent with the hormonal pleiotropy hypothesis, these effects on reproduction were further matched by subtle shifts in the CHC profiles, with univariate analyses showing that in P. dominula and P. satan the abundance of particular linear alkanes and mono-methylated alkanes were affected by ovary development and our hormonal treatments. The results indicate that in primitively eusocial wasps, and particularly in Polistes, reproduction and the production of some CHC cues are under joint JH control. We suggest that pleiotropic links between reproduction and the production of such hydrocarbon cues have been key enablers for the origin of true fertility and queen signals in more derived, advanced eusocial insects.

Keywords: Polistinae wasps; cuticular hydrocarbons; fertility cues; juvenile hormone; queen pheromones.

Figure 1.

Representative pictures of the three categories of ovary activation found per species. (A) Not activated. (B) Half activated. (C) Fully activated. 1, Polistes dominula; 2, Polistes satan; 3, Mischocyttarus metathoracicus; and 4, Mischocyttarus cassununga.

Figure 2.

JH has a gonadotropic effect across four primitively eusocial paper wasps. Mean worker ovary activation observed 10–12 days following treatment with the JH analog methoprene and the anti-JH precocene compared with in the acetone solvent control condition in the four paper wasp study species (Polistes dominula, Polistes satan, Mischocyttarus metathoracicus, and Mischocyttarus cassununga). Ovaries were scored on a three-level ordinal scale, ranging from not activated (1) to half activated (2) or fully activated (3). Fitted values of a main effects CLMM with nest coded as a random factor with 95% confidence intervals, N = number of nests, n = total number of individuals treated. Across the four species, precocene significantly decreased ovary development when compared with both the acetone solvent-only control (z-ratio = 2.35, P = 0.02*) and the methoprene treatment (z-ratio = 2.96, **P = 0.003). The pairwise between acetone and methoprene was not different (z-ratio = −0.75, P = 0.45) (Table 2C).

Figure 3.

Heatmap showing differences in relative abundance of compounds (log-transformed) in the chemical profiles of Polistes dominula females from the three treatments—methoprene, acetone, and precocene. Colors indicate the mean fold difference in relative abundance of each hydrocarbon on the cuticular body surface of treated females. Compounds were clustered based on a UPGMA hierarchical clustering using Euclidean distance as the distance metric. Asterisks indicate the FDR-corrected significances of groups’ contrasts (***P < 0.001, **P < 0.01, *P < 0.05).

Figure 4.

Heatmap showing differences in relative abundance of compounds (log-transformed) in the chemical profiles of Polistes satan females from the three treatments—methoprene, acetone, and precocene. Colors indicate the mean fold difference in relative abundance of each hydrocarbon on the cuticular body surface of treated females. Compounds were clustered based on a UPGMA hierarchical clustering using Euclidean distance as the distance metric. Asterisks indicate the FDR-corrected significances of groups’ contrasts (***P < 0.001, **P < 0.01, *P < 0.05).

Figure 5.

(A) Heatmap showing differences in relative abundance of compounds (log-transformed) in the chemical profiles of Mischocyttarus metathoracicus females from the three treatments—Methoprene, acetone, and precocene. (B) Heatmap showing differences in relative abundance of compounds (log-transformed) in the chemical profiles of Mischocyttarus cassununga females. Colors indicate the mean fold difference in relative abundance of each hydrocarbon on the cuticular body surface of treated females. Compounds were clustered based on a UPGMA hierarchical clustering using Euclidean distance as the distance metric. Asterisks indicate the FDR-corrected significances of individual contrasts (***P < 0.001, **P < 0.01, *P < 0.05).