Multiple nuptial flights, sperm transfer and the evolution of extreme polyandry in honeybee queens

The honeybee, Apis mellifera, has an extremely polyandrous mating system, which often involves multiple nuptial flights by its queens. To understand the evolution of extreme polyandry, we investigated the cost of multiple nuptial flights in relation to potential benefits. We analysed, with eight DNA microsatellite loci, the paternity of worker offspring of naturally mated queens. Queens that were restricted to one nuptial flight, but may have taken additional nuptial flights if allowed to do so, had significantly fewer matings than queens that started oviposition after a single nuptial flight. Furthermore, the number of sperm stored in a spermatheca increased significantly with the number of matings. We suggest that queens adjust their nuptial flight frequencies according to their mating success in their previous nuptial flights. The number of copulations seems to serve as a signal for the initiation of oviposition. In the light of these findings, we reconsider and discuss the significance of the sperm limitation hypothesis for the evolution of extreme polyandry in A. mellifera.