Social Hymenoptera are characterized by a reproductive division of labor, whereby queens perform most of the reproduction and workers help to raise her offspring. A long-lasting debate is whether queens maintain this reproductive dominance by manipulating their daughter workers into remaining sterile (queen control), or if instead queens honestly signal their fertility and workers reproduce according to their own evolutionary incentives (queen signaling). Here, we test these competing hypotheses using data from Vespine wasps. We show that in natural colonies of the Saxon wasp, Dolichovespula saxonica, queens emit reliable chemical cues of their true fertility and that these putative queen signals decrease as the colony develops and worker reproduction increases. Moreover, these putative pheromones of D. saxonica show significant conservation with those of Vespula vulgaris and other Vespinae, thereby arguing against fast evolution of signals as a result of a queen–worker arms race ensuing from queen control. Lastly, levels of worker reproduction in these species correspond well with their average colony kin structures, as predicted by the queen signaling hypothesis but not the queen control hypothesis. Altogether, this correlative yet comprehensive analysis provides compelling evidence that honest signaling explains levels of reproductive division of labor in social wasps.

sponsorship: We are grateful to K.R. Foster for providing us with the original data of his studies of Vespine wasps and to all members of the Copenhagen Centre for Social Evolution for providing a stimulating working environment. JSvZ and PdE were supported by a postdoctoral fellowship from the Danish Council for Independent Research (FNU 09-066595) and an EU Marie Curie Excellence Grant CODICES-EXT-CT-2004-014202. WB and TW were supported by the Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen), the Research Foundation Flanders (FWO GNM-B5996-KAN2006), and the Centre of Excellence funding by the KU Leuven Research Fund (PF/2010/007). (Danish Council for Independent Research|FNU 09-066595, EU Marie Curie Excellence Grant|CODICES-EXT-CT-2004-014202, Institute for the Promotion of Innovation through Science and Technology in Flanders (IWT-Vlaanderen), Research Foundation Flanders|FWO GNM-B5996-KAN2006, Centre of Excellence, KU Leuven Research Fund|PF/2010/007)