A virgin honey bee queen mates early in her life, having sex "on the fly" with as many as twenty drones over a period of a few days, and then she never mates again. She produces eggs throughout her life in well-developed ovaries that fill up most of her abdomen, and she can produce hundreds of thousands of offspring in her lifetime from the sperm she stores in those few days.
A few days after the young honey bee queen has emerged from her pupal case, she flies to a so-called drone congregation area, where a large number of fertile males from nearby colonies are assembled, waiting to take advantage of their once-in-alifetime opportunity to pass on their genes to any virgin queen that comes along. The drones fly around at a height of twenty or thirty feet above the ground, and they locate a receptive queen by sensing her pheromones and by using all five of their eyes. If they are vigorous enough to catch up with a queen, they may get the opportunity to indulge in what has been described as an "acrobatic orgy."
Once contact has been made, the mating generally lasts from one to five seconds. "Within a split second, the drone grasps the queen with all six legs and everts the endophallus into the queen's open sting chamber. At this point the drone becomes paralyzed and flips backward, and ejaculation results from the pressure of the drone's hemolymph as the abdomen contracts. The explosive and sometimes audible ejaculation ruptures the everted endophallus and propels the semen through the queen's sting chamber and into her oviduct". The ejaculation separates the drone from the queen, and he dies shortly after mating.
Observers report that they can tell when a queen bee is mating nearby because of the large number of dying drones that drop to the ground, sometimes accompanied by a noise like popcorn popping. The drone's severed genitals may act as a temporary vaginal plug, designed to allow time for the drone's sperm to enter the queen's system, but the queen or a subsequent suitor can dislodge the plug, so no drone is guaranteed exclusivity.
The queen receives an average of six million sperm from each male, but sperm die in large numbers as they make their way through the female's reproductive tract, and some may be ejected during the course of a subsequent mating. Stored sperm may even be digested in lieu of food in times of famine, so, typically, the queen will retain only about six million sperm from this mass mating to fertilize her eggs. In fact, this multiple mating (polyandry) assures genetic diversity that confers multiple benefits on the colony .
In some solitary species of the genera Nomadopsis and Perdita, the male may remain coupled with the female while she forages or flies back to the nest after mating, preventing other males from mating with her. Centris adani males deposit pheromones on the female during mating that repel other males. Male bees in these species also die shortly after mating, and the female begins searching for a place to build a nest. Some solitary females only mate shortly after they emerge from the pupal stage.
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