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 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.
Highlights
One of the defining characteristics of eusociality is the spectacular reproductive division of labor between fertile queens and mostly nonreproductive workers[1]
It has been suggested that the convergent evolution of hydrocarbon queen pheromones across several independently evolved lineages may be driven by the fact that specific cuticular hydrocarbon compounds (CHCs) tend to correlate with reproductive state in both social and non-social insect species[10,11,12,13,14,15,16], and that this would predispose them to be co-opted as honest signals of fertility[10, 17,18,19]
To test if juvenile hormone (JH), which typically acts as a gonadotropin in wasps[26, 27, 29, 34, 38, 56], controls the production of queen- or fertility-linked cuticular hydrocarbon signals, we performed experiments in which we treated common wasp workers that had been isolated from their mother queen with the JH analog methoprene and the JH inhibitor precocene-51, 52
Summary
One of the defining characteristics of eusociality is the spectacular reproductive division of labor between fertile queens and mostly nonreproductive workers[1]. The way in which this tight linkage between fertility and the production of specific hydrocarbons signals would come about is still under debate, but one popular theory has suggested that this could be explained by fertility and hydrocarbon signal production being under shared endocrine control[13] In support of this hypothesis based on “hormonal pleiotropy”[20], it has been shown that the production of fertility-linked cuticular compounds is under juvenile hormone (JH) in fruit flies[21], cockroaches[22] and burying beetles[23] as well as in primitively eusocial Ponerine ants[17, 24] and Polistine wasps[25,26,27], and that juvenile hormone plays a key role in the reproduction of several of these species by acting as a gonadotropin[27,28,29,30,31]. We determine if JH acts as a gonadotropin in queens or workers in this species by comparing the JH hemolymph titers of reproductive queens with that of non-reproductive virgin queens and non-reproductive workers, as well as by testing whether the methoprene or precocene-I treatments affected the workers’ ovary development
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