Promiscuous Honey Bee Queens Increase Colony Productivity by Suppressing Worker Selfishness

Queen monogamy is ancestral among bees, ants, and wasps (Order Hymenoptera), and the close relatedness that it generates within colonies is considered key for the evolution of eusociality in these lineages [1]. Paradoxically, queens of several eusocial species are extremely promiscuous [2], a derived behavior that decreases relatedness among workers and fitness gained from rearing siblings but benefits queens by enhancing colony productivity [3–9] and inducing workers to rear queens’ sons instead of less related worker-derived males [10–13]. Selection for promiscuity would be especially strong if productivity in a singly inseminated queen’s colony declined because selfish workers invested in personal reproduction at the expense of performing tasks that contribute to colony productivity. We show in honey bees that workers’ ovaries are more developed when queens are singly rather than multiply inseminated and that increasing ovary activation is coupled with reductions in task performance by workers and colony-wide rates of foraging and waggle-dance recruitment. Increased investment in reproductive physiology by selfish workers might result from greater incentive for them to favor worker-derived males or because low mating frequency signals a queen’s diminished quality or future fecundity. Either possibility fosters selection for queen promiscuity, revealing a novel benefit of it for eusocial insects. ► More workers have developed ovaries when queens have mated singly, not multiply ► Colony-level foraging and dancing activity declines as ovary activation increases ► Workers with activated ovaries are less likely to perform critical colony tasks ► A novel benefit of polyandry is greater productivity from more unselfish workers