When does cheating pay? Worker reproductive parasitism in honeybees

Abstract

The notion that honeybee colonies are harmonious, isolated societies in which workers selflessly sacrifice their reproductive opportunities to serve their queen has long been debunked. Like any society, honeybee colonies contain selfish individuals that pursue their own interests, or cheat, at the expense of the colony, and these individuals need to be controlled. There are numerous studies detailing the myriad ways in which selfish workers may subvert the typical dominance hierarchy of a haplo-diploid insect society. Recent studies have focussed on thelytoky, the ability to produce diploid offspring without mating, as the most significant attribute of a successful reproductive parasite. However, we argue that thelytoky is not necessary for successful parasitism, and that even arrhenotokous societies contain specialized reproductive parasites. Using A. mellifera and A. cerana as examples, we show that the most important aspects of a would-be reproductive cheat’s success are an ability to escape policing and the timing of the reproductive attempt. Finally, we show that thelytoky, while not necessary for the evolution of successful reproductive parasites, can give rise to specialized parasitic lineages and that such lineages are likely to be far more common than previously assumed.