Sexual selection in honey bees: colony variation and the importance of size in male mating success

Sexual selection is a dominant force in the evolution of many animals and can be particularly significant in species that mate in aerial swarms characterized by strong male male competition. However, such mating biology, typical of many social insects, is also quite challenging to study. Here, we investigate sexual selection in the honey bee that has 2 distinct male morphs (normal sized and small). Males mate only once and females return to their nest after mating, making it possible to measure the lifetime fitness of both sexes. We allowed known numbers of normal-sized males from 6 colonies and small males from another 6 colonies to compete for natural matings with experimental virgin queens. We then determined the mating success of males by genotyping the offspring of these queens. Colonies differed by an order of magnitude in the intrinsic mating success of their males, confirming that the reproductive fitness of honey bee colonies is highly variable. Small males achieved approximately half as many matings as expected given their number of flights and, in addition, had a significantly smaller share of paternity per mating than normal-sized males. Interestingly, the flight activity of small males suggested that they may compensate for their lower competitiveness by flying outside the most competitive mating period in the afternoon. The lower fitness of small males shows that sexual selection is strong in honey bees and contributes to inclusive fitness dynamics that favor worker cooperation within their societies.