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Multiple mating (and insemination) by females with different males, polyandry, is widespread across animals, due to material and/or genetic benefits for females. It reaches particularly high levels in some social insects, in which queens can produce significantly fitter colonies by being polyandrous. It is therefore a paradox that two thirds of eusocial hymenopteran insects appear to be exclusively monandrous, in spite of the fitness benefits that polyandry could provide. One possible cost of polyandry could be sexually transmitted parasites, but evidence for these in social insects is extremely limited. Here we show that two different species of  Nosema  microsporidian parasites can transmit sexually in the honey bee  Apis mellifera . Honey bee males that are infected by the parasite have  Nosema  spores in their semen, and queens artificially inseminated with either  Nosema  spores or the semen of  Nosema -infected males became infected by the parasite. The emergent and more virulent  N. ceranae  achieved much higher rates of infection following insemination than did  N. apis . The results provide the first quantitative evidence of a sexually transmitted disease (STD) in social insects, indicating that STDs may represent a potential cost of polyandry in social insects.

The cost of promiscuity: sexual transmission of Nosema microsporidian parasites in polyandrous honey bees