Honey bee queen mandibular pheromone inhibits ovary development and fecundity in a fruit fly

Abstract

A key feature of eusocial insects is their reproductive division of labour. The queen signals her fecundity to her potentially reproductive daughters via a pheromone, which renders them sterile. In contrast, solitary insects lack division in reproductive labour and there is no such social signalling or need for ovary‐regulating pheromones. Nonetheless, females from both non‐social and eusocial lineages are expected to regulate their ovaries to maximize inclusive lifetime reproductive success. It is not known, however, whether the underlying networks that regulate ovary activation are homologous between non‐social and eusocial taxa, especially when these taxa are phylogenetically distant. In this study, we provide evidence that solitary fruit flies may share a conserved ovary‐regulating pathway with a eusocial honey bee, Apis mellifera L. (Hymenoptera: Apidae). Specifically, we demonstrate that honey bee queen mandibular pheromone (QMP) inhibits fly ovaries in much the same way as it suppresses worker ovaries. Drosophila melanogaster Meigen (Diptera: Drosophilidae) exposed to sufficient doses of QMP showed a reduction in ovary size, produced fewer eggs, and generated fewer viable offspring, relative to unexposed controls. Drosophila melanogaster therefore responds to an interspecific social cue to which it would not normally be exposed. Although we cannot strictly rule out an incidental effect, this conspicuous response suggests that these two species may share an underlying mechanism for ovary regulation. Why a non‐social species of fly responds to a highly social bee's pheromone is not clear, but one possibility is that solitary and social insects share pathways associated with female reproduction, as predicted by the ‘groundplan’ hypothesis of social evolution.

A novel screen for genes associated with pheromone-induced sterility

“…4C,D). Why olfactory receptive flies respond to bee pheromone is an open question1314, with one possibility being that social insect queen pheromones act on conserved regulatory pathways that were already present in solitary ancestors24. Regardless, our tetanus toxin-based validation suggests that the original RNAi screen did capture a functional subset of receptors with a capacity to perceive the ovary-inhibiting pheromone.…”

“…We reason that if female flies consume roughly 2 μl of food per day then the oral dose of QMP would be ~1.3 queen equivalents (13 QE in 20 μl @ 2 μl = 1.3 QE), or less via olfaction alone. Therefore, the effective dose is estimated to be within a biologically relevant range that has been shown to effectively suppress fly ovaries in a manner comparable to its normal effect on worker bees14. Moreover, the effect of pheromone treatment at these doses does appear to specifically affect fly ovaries, as opposed to other aspects of female reproduction (pupation) or survivorship14.…”

“…14. We synchronized adult emergence by first housing (for 24 hrs) a small reproductive population (n = 30 males and n = 30 females) in collection cages (60 mm; Diamed, Mississauga, Canada) fitted with nutrient (grape juice and agar) plates.…”

“…Therefore, the effective dose is estimated to be within a biologically relevant range that has been shown to effectively suppress fly ovaries in a manner comparable to its normal effect on worker bees14. Moreover, the effect of pheromone treatment at these doses does appear to specifically affect fly ovaries, as opposed to other aspects of female reproduction (pupation) or survivorship14. Lack-of-response to a control pheromone (7-triclosene), and variable response among reproduction-related genotypes13, further suggests that this ovary-specific response is not simply a pharmacological side-effect to a pheromone of any type.…”

“…We have recently discovered however that application of QMP to virgin fruit flies suppresses fecundity in a manner comparable to its normal effect on honeybees. Treated flies tend to have smaller ovaries that contain fewer mature eggs1314. This worker-like response from Drosophila melanogaster (Diptera) to a eusocial honeybee (Hymenoptera) pheromone implies conserved reproductive regulation between social and pre-social orders and introduces Drosophila as a proxy model for the action of sterility-inducing pheromones15.…”