Multiple mating by females (polyandry) is taxonomically widespread but the evolution of such behaviors is not clearly understood given potential costs of polyandry such as time, energy, or predation risk. The genetic variability versus parasites hypothesis predicts a reduction of parasitism due to increased genetic variability among offspring and an associated fitness gain. We tested this hypothesis with a field experiment in the bumblebee, Bombus terrestris L. Worker heterogeneity within the colony was experimentally altered by artificially inseminating queens with sperm from one male, four brothers, two males, or four unrelated males. We found genetic variability to be effective, because intensity and prevalence of the most common parasite, Crithidia bombi, a trypanosome, decreased with increasing levels of colony heterogeneity. Fitness differed between treatments but did not increase in a simple way, with increasing genetic heterogeneity among colony workers. Instead, fitness followed a U-shaped function with a minimum for small amounts of genetic heterogeneity. We therefore suggest that polyandry also induces a cost, perhaps as a result of the social structure within the colony. In evolutionary terms, singly mated females appear to be constrained by an adaptive valley that needs to be crossed before high degrees of mating frequency can be reached. This may help to explain why B. terrestris and most other social insects are often monandrous.

Corresponding Editor: D. Wheeler