Hormonal pleiotropy helps maintain queen signal honesty in a highly eusocial wasp

Authors: OLIVEIRA, RICARDO - Katholieke University; VOLLET-NETO, AYRTON - Katholieke University; OI, CINTIA - Katholieke University; VAN ZAWEDEN, JELLE - Katholieke University; NASCIMENTO, FABIO - Universidade De Sao Paulo; Brent, Colin; WENSELEERS, TOM - Katholieke University

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/10/2017
Publication Date: 6/10/2017
Publication URL: http://handle.nal.usda.gov/10113/5700727
Citation: Oliveira, R.C., Vollet-Neto, A., Oi, C.A., Van Zaweden, J.S., Nascimento, F., Brent, C.S., Wenseleers, T. 2017. Hormonal pleiotropy helps maintain queen signal honesty in a highly eusocial wasp. Scientific Reports. 7:1654.

Interpretive Summary: In the common wasp Vespula vulgaris, the compositions of the waxy compounds coating the cuticles of queens and workers are very different. In a number of socially complex species, such as ants and termites, the compounds act as signals of fertility, but there is debate as to whether these signals could be mimicked by cheating workers. We hypothesized that queen fertility signals could be uncheatable if their production would be under the control of juvenile hormone (JH), a key endocrine regulator in insects that plays central roles in caste determination and reproduction. To test this hypothesis, we first determined that JH was very low in workers and reproductively inactive virgin queens, but very high in egg-laying queens. Artificially elevating the levels of JH in workers caused these individuals to express cuticlar compounds that were normally only found on fertile queens. Applying precocene, a substance that impairs JH function, was able to block the production of these queen-specific compounds. Furthermore, observed differences in JH levels support a strong link between hormonal state and egg production. While workers and virgin, non-egg-laying queens, had relatively low levels of the hormone, egg laying queens had substantially higher levels. Overall, these results suggest that queen signal honesty in this system is maintained by queen fertility and queen signal production being under shared endocrine control.

Technical Abstract: In insect societies, both queens and workers produce chemicals that reliably signal caste membership and reproductive status. The mechanisms that help to maintain the honesty of such queen and fertility signals, however, remain poorly studied. Here we test if queen signal honesty could be based on the shared endocrine control of queen fertility and the production of specific signals. In support of this “hormonal pleiotropy” hypothesis, we find that in the common wasp, application of methoprene (a juveline hormone analogue) caused workers to acquire a queen-like cuticular hydrocarbon profile, resulting in the overproduction of known queen pheromones as well as of some compounds typically linked to worker fertility. By contrast, administration of precocene-I (a JH inhibitor) had a tendency to have the opposite effect. Furthermore, a clear gonadotropic effect of JH in queens was suggested by the fact that circulating levels of JH were ca. 2 orders of magnitude higher in queens than those in workers and virgin, non-egg-laying queens, even if methoprene or precocene treatment did not affect the ovary development of workers. Overall, these results suggest that queen signal honesty in this system is maintained by queen fertility and queen signal production being under shared endocrine control.