Mating takes place about 20 to 50 feet in the air, well above the normal flight path of worker honey bees, which is about eight feet above the ground. Workers are antagonistic toward all foreign queens and will attack and ball any queens they encounter outside of their hive. Strong winds will force queens and drones as well as worker bees to fly closer to the ground. Drones fly from one congregation area to another searching for virgin queens, and will take more than one flight a day in an attempt to find a queen.
To mate, a drone approaches a queen from behind and grasps her abdomen with its legs. The mating act itself is brief. Drones possess genitalia that are larger in proportion to their body size than all other animal species except a few species of fleas. The drone genitalia are contained in the abdomen. When they are everted, a popping sound can be heard. The shock of everting the genitalia results in the death of the male, which falls over backwards and to the ground. At this stage the genitalia may be separated from the male and remain in the queen, but usually only briefly. Apparently the queen removes them herself and continues to mate with other drones. Queens usually take two or three mating flights; one study indicates that queens will continue to search for males until they receive sufficient sperm to fill their spermathecae. All of the older textbooks and papers on honey bees state that queens mate once, rarely twice. In 1954 Taber III found that queen honey bees mate several times; he believed this number was seven or eight, but more recent studies have shown that the averge queen probably mates with 15 to 17 drones within one to two days when she is three to five days old. Apparently queens are unable to mate after the age of about 20 – 30 days. Drones are not mature and capable of mating until about 12 days of age.
In the process of mating, a queen collects about five million sperm that are packed into a pouch in her abdomen called the spermatheca. This is a curiosity since an individual drone carries about twice that number of sperm. As an egg passes down from the ovaries to be deposited in a cell, a few sperm are released and one enters the egg and fertilizes it. These eggs develop into worker bees and rarely queens. Drone eggs are not fertilized, and it is not known how the queen controls this. The supply of sperm obtained when the queen is young usually lasts the rest of her life and she never mates again.
The only other time a queen will leave a hive, other than to mate, is to accompany a swarm to a new home site.