In the highly eusocial wasp, Vespula vulgaris, queens produce honest signals to alert their subordinate workers of their fertility status, and therefore they are reproductively suppressed and help in the colony. The honesty of the queen signals is likely maintained due to hormonal regulation, which affects fertility and fertility cue expression. Here, we tested if hormonal pleiotropy could support the hypothesis that juvenile hormone controls fertility and fertility signaling in workers. In addition, we aimed to check oocyte size as a proxy of fertility. To do that, we treated V. vulgaris workers with synthetic versions of juvenile hormone (JH) analogue and a JH inhibitor, methoprene and precocene, respectively. We dissected the treated females to check ovary activation and analyzed their chemical profile. Our results showed that juvenile hormone has an influence on the abundance of fertility linked compounds produced by workers, and it also showed to increase oocyte size in workers. Our results corroborate the hypothesis that juvenile hormone controls fertility and fertility signaling in workers, whereby workers are unable to reproduce without alerting other colony members of their fertility. This provides supports the hypothesis that hormonal pleiotropy contributes to keeping the queen fertility signals honest.

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 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 (juvenile hormone) 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 to 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 cuticular hydrocarbon 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.

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The buff-tailed bumblebee Bombus terrestris presents two distinct colony phenotypes in which some colonies already start producing males very early in the season, while others switch to producing sexuals much later in the season, and specialize mainly in the production of virgin queens. Despite having been extensively investigated in the past, the mechanisms underlying these two distinct phenotypes remain poorly understood. Here we use a combination of behavioral and genetic data to demonstrate that early switchers are in fact diploid male producing colonies, while late switchers produced normal, haploid males. Hence, at a proximate level, early switching to male production was caused by queens mating with males that by chance carried the same sex allele. These patterns were not the result of strong inbreeding within the study population, as the average inbreeding coefficient was very low and in fact slightly negative (−0.11). Moreover, an effect of inbreeding was further excluded because hybrids produced by crossing two distinct outbred populations also produced diploid males in early switching colonies. Finally, we found that diploid males only emerged after a first cohort of workers was produced, while we would have expected diploid males to be produced simultaneously with workers in a 50:50 ratio. We demonstrate that adult diploid males had a distinct cuticular hydrocarbon profile and propose that queens likely cull diploid males during early colony development to reduce the cost of diploid male production.