To house or oust: Honey bee (Apis mellifera) colonies can evaluate and evict drones of low quality

Abstract

Abstract Across the animal kingdom, males advertise their quality to potential mates. Males of low reproductive quality, such as those that are sick, may be excluded from mating. In eusocial species, there is some evidence that reproductive females gauge the quality of their mates. However, males often spend much more time with non-reproductive females when being raised or when returning from unsuccessful mating flights. Do non-reproductive workers evaluate the quality of male reproductives? Here we address this question using male honey bees (Apis mellifera), called drones, as a model. We generated immune-challenged drones by injecting them with lipopolysaccharide and tested: 1) do workers evict immune-challenged drones from their colony, 2) do cuticular hydrocarbon (CHC) profiles, body size, or mass change when drones are immune-challenged, and 3) are these changes used by workers to exclude low quality males from the colony? We found that an immune challenge causes changes in CHC profiles of drones and reduces their body mass. Workers selectively evict small and immune-challenged drones who, themselves, do not self-evict. This work demonstrates that some eusocial males undergo an additional layer of scrutiny prior to mating mediated by the non-reproductive worker caste. Significance statement Males of some species must advertise their quality to mates but, in the case of eusocial species, must they also advertise their quality to nestmates? By manipulating honey bee male quality, we found that small and immune-challenged drones are evicted from colonies overnight. Workers may not use a drone’s cuticular hydrocarbon profile to make this assessment. This is a new example of social immunity expressed against adult males and an example of worker involvement in reproductive decisions.