Behavior, ovarian status, and juvenile hormone titer in the emblematic social wasp Zethus miniatus (Vespidae, Eumeninae)

Showing traces of eusocial behavior, Zethus miniatus is an emblematic member of the primarily solitary subfamily Eumeninae. The females of this casteless species share a common nest, but each one provisions her own brood in a progressive manner. They express dominance when reproductive (queen-like behavior) and occasionally perform tasks that benefit others when provisioning the brood (worker-like behavior). Hence, the biology of this species has long been considered as harboring traits that could mark the transition from a solitary to social lifestyle. Here, we present for the first time measurements of the juvenile hormone (JH) titer in combination with behavioral observations and data on the females' ovarian status. Aggressive reproductives seeking to reuse or usurp brood cells were found to possess longer oocytes than provisioners of young larvae. Brood killings by reproductive cell-seekers and JH titers were both higher when the female/open-brood-cell ratio of the nest was high-an indicator of strong competition. Females lacking brood, such as those that are victims of cell usurpation attempts by other females, were found to perform tasks relating to nest defense, nest maintenance, and/or adoption of orphaned brood. Hence, we hypothesize that competition for brood cells may have shaped the reproductive physiology of this group-living species of social wasps, and that JH is critical for this competitive behavior. Furthermore, we hypothesize that JH-mediated dominance interactions in casteless groups may have preceded and contributed to the origin of reproductive castes.Significance statementHow, mechanistically, did caste phenotypes (a polyphenism with egg-layers and non-egg-laying helper females within groups) originate from solitary ancestors? Key to addressing this question can be casteless, group-living wasp species, where the females progressively feed their brood. The eumenine wasp Zethus miniatus has behavioral traits intermediate between solitary and caste-possessing wasps, and hence, has gained a model status for this transition. This is the first study of such a wasp in nature that combines data on behavior, ovarian activity, and juvenile hormone (JH) levels. The results show that the ovarian status of a Z. miniatus female is a good predictor of her behavior, and that JH titers were highest when competition for available brood cells was intense. This suggests that JH may have become linked to the origin of worker caste behaviors through its involvement in competitive interactions among nestmates.

Automated summary

Zethus miniatus is a predominantly solitary wasp species that exhibits some eusocial behavior. The females share a nest but provision their own brood. They display queen-like behavior when reproductive and worker-like behavior when provisioning the brood. This study provides insights into the reproductive physiology and behavior of this group-living species and suggests a link between competition for brood cells and the origin of reproductive castes.