Effects of juvenile hormone in fertility and fertility-signaling in workers of the common wasp Vespula vulgaris

Abstract

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.

Juvenile hormone affects age polyethism, ovarian status and cuticular hydrocarbon profile in workers of the waspPolybia occidentalis

“…In social wasps, JH has been shown to influence transitions between worker tasks by accelerating the behavioral ontogeny in experimentally treated individuals (O'Donnell and Jeanne, 1993;Chang et al, 2015;Giray et al, 2005;Shorter and Tibbetts, 2009;Tibbetts et al, 2013). As JH also causes an increase in the oocyte length of workers by acting as an ovarian activator (Kelstrup et al, 2014b;Oi et al, 2021), both reproductive and behavioral traits are controlled by the same endocrine pathway (O'Donnell and Jeanne, 1993;Kelstrup et al, 2014b). Furthermore, JH also appears to be involved in regulating pheromone production, such as the cuticular hydrocarbon (CHC) profiles of queens and workers (Robinson and Vargo, 1997;Oliveira et al, 2017).…”

Role of Endocrine System in the Regulation of Female Insect Reproduction

“…The results showed that the oocyte size was increased after treatment with the methoprene; nevertheless, oocyte size was decreased against precocene. Thus, JH affects both fertility and fertility signaling in workers [66].…”

Juvenile hormone modulates hydrocarbon expression and reproduction in the german wasp Vespula germanica

“…In swarm-founding species, JH has been reported to control behavioral maturation in Polybia occidentalis (Prato et al, 2021), and ovary activation and chemical expression of CHCs in P. occidentalis (Prato et al, 2021) and Synoeca surinama (Kelstrup et al, 2014). In highly eusocial wasps, JH effects have been well studied so far in a single species, namely Vespula vulgaris, and one of the roles is being associated with regulating reproductive traits in females, leading to modification of certain cuticular compounds over the cuticle (Oliveira et al, 2017;Oi et al, 2020Oi et al, , 2021a. By treating workers topically with a JH analog (methoprene), studies in the past have supported that in addition to the regulation of CHC production, JH may be directly responsible for increasing the proportion of queen pheromones in V. vulgaris (the compounds n-C27, n-C28, n-C29, and 3-MeC29) (Oliveira et al, 2017;Oi et al, 2021a).…”

“…In highly eusocial wasps, JH effects have been well studied so far in a single species, namely Vespula vulgaris, and one of the roles is being associated with regulating reproductive traits in females, leading to modification of certain cuticular compounds over the cuticle (Oliveira et al, 2017;Oi et al, 2020Oi et al, , 2021a. By treating workers topically with a JH analog (methoprene), studies in the past have supported that in addition to the regulation of CHC production, JH may be directly responsible for increasing the proportion of queen pheromones in V. vulgaris (the compounds n-C27, n-C28, n-C29, and 3-MeC29) (Oliveira et al, 2017;Oi et al, 2021a). Furthermore, in V. vulgaris, increasing JH levels may be decisive for reproductive workers to succeed (Oi et al, 2020), as workers treated with methoprene lay eggs that chemically resemble those laid by queens, and in doing so, their eggs were less policed (Oi et al, 2020).…”

“…Besides that, Dufour's gland compounds are used during nest building, nestmate recognition, fertility signaling, brood cell lining, and as sexual pheromones (Mitra, 2013). Given the existing evidence that V. vulgaris workers treated with methoprene lay eggs that chemically resemble those laid by the queens (Oi et al, 2020), it is likely that increasing JH levels have cascade effects, that not only trigger cuticle chemical modification (Oi et al, 2021a) but also trigger a modification in other chemical reservoirs, such as the Dufour's gland. Hence, the chemical modification in the eggs laid by methoprene-treated workers in V. vulgaris may represent a modification in Dufour's gland composition.…”