Variation in the reproductive quality of honey bee males affects their age of flight attempt

Honey bee males (drones) exhibit life histories that enable a high potential for pre- or post-copulatory sperm competition. With a numerical sex ratio of ∼11,000 drones for every queen, they patrol flyways and congregate aerially to mate on the wing. However, colonies and in fact drones themselves may benefit from a relative lack of competition, as queens are highly polyandrous, and colonies have an adaptive advantage when headed by queens that are multiply mated. Previous research has shown that larger drones are more likely to be found at drone congregation areas, more likely to mate successfully, and obtain a higher paternity share. However, the reproductive quality and size of drones varies widely within and among colonies, suggesting adaptive maintenance of drone quality variation at different levels of selection.

We collected drones from six colony sources over the course of five days. We paint marked and individually tagged drones after taking body measurements at emergence and then placed the drones in one of two foster colonies. Using an entrance cage, we collected drones daily as they attempted flight. We collected 2,420 drones live or dead, analyzed 1,891 for attempted flight, collected emergence data on 207 drones, and dissected 565 upon capture to assess reproductive maturity. We measured drone body mass, head width, and thorax width at emergence, and upon dissection we further measured thorax mass, seminal vesicle length, mucus gland length, sperm count, and sperm viability from the seminal vesicles.

We found that drones that were more massive at emergence were larger and more fecund upon capture, suggesting that they are of higher reproductive quality and therefore do not exhibit a trade-off between size and fecundity. However, smaller drones tended to attempt initial flight at a younger age, which suggests a size trade-off not with fecundity but rather developmental maturation. We conclude that smaller drones may take more mating flights, each individually with a lower chance of success but thereby increasing their overall fitness. In doing so, the temporal spread of mating attempts of a single generation of drones within a given colony increases colony-level chances of mating with nearby queens, suggesting an adaptive rationale for high variation among drone reproductive quality within colonies.