Males vs workers: testing the assumptions of the haploid susceptibility hypothesis in bumblebees

The haploid state of males in eusocial Hymenoptera—the ants, bees, and wasps—has been proposed as a driving force in the evolution of social behavior under the assumption that haploidy results in higher susceptibility to pathogens. In this study, we present the first test of the assumptions of the “haploid male susceptibility hypothesis”. We challenged males and workers of the bumblebee Bombus terrestris with its parasite Crithidia bombi but found no differences in either initial susceptibility or the intensity of infection between haploid males and diploid females. We reviewed observational studies on parasitism in haplodiploid insects and found that in 15 out of 26 cases, haploid males had lower parasite prevalence. However, the majority of available data related to nontransmissible parasites and thus any general statements about haploid susceptibility remain unclear. Using a simulation model, we studied how diverse genetic mechanisms could affect the values for resistance; results suggest that only a phenomenon that renders workers effectively haploid, e.g., imprinting, could explain our experimental results. A more likely explanation is that, in eusocial Hymenoptera with predominantly female populations, parasites may simply become more adapted to the more common female hosts and, thus, male haploid susceptibility may be hidden due to parasite adaptation. Our results do not support the idea that the haploid susceptibility hypothesis explains the origin or maintenance of social systems in the eusocial Hymenoptera.