Abstract

For honey bee and other social insect colonies the ‘queen substance’ regulates colony reproduction rendering workers functionally sterile. The evolution of worker reproductive altruism is explained by inclusive fitness theory, but little is known of the genes involved or how they regulate the phenotypic expression of altruism. We previously showed that application of honeybee queen pheromone to virgin fruit flies suppresses fecundity. Here we exploit this finding to identify genes associated with the perception of an ovary-inhibiting social pheromone. Mutational and RNAi approaches in Drosophila reveal that the olfactory co-factor Orco together with receptors Or49b, Or56a and Or98a are potentially involved in the perception of queen pheromone and the suppression of fecundity. One of these, Or98a, is known to mediate female fly mating behaviour, and its predicted ligand is structurally similar to a methyl component of the queen pheromone. Our novel approach to finding genes associated with pheromone-induced sterility implies conserved reproductive regulation between social and pre-social orders, and further helps to identify candidate orthologues from the pheromone-responsive pathway that may regulate honeybee worker sterility.

Highlights

  • For honey bee and other social insect colonies the ‘queen substance’ regulates colony reproduction rendering workers functionally sterile

  • The evolution of worker reproductive altruism is explained by inclusive fitness theory, but little is known of the genes involved or how they regulate the phenotypic expression of altruism

  • We previously showed that application of honeybee queen pheromone to virgin fruit flies suppresses fecundity

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Summary

Introduction

For honey bee and other social insect colonies the ‘queen substance’ regulates colony reproduction rendering workers functionally sterile. Individual ORs that block the fly’s conspicuous worker-like response to QMP represent functional candidates for the olfactory perception of ovary-inhibiting queen pheromone. To the extent that receptors identified from the fly are homologous to those from the bee, we use our Drosophila model to identify, for the first time, candidates from the pheromone-responsive pathway that may regulate honeybee worker sterility.

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