The Gene vitellogenin Has Multiple Coordinating Effects on Social Organization

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Abstract
Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes. Animals that live in groups often specialize in different tasks, creating a division of labor. One extreme example can be seen in honeybees, in which most tasks are performed by thousands of worker females that are essentially sterile helpers. Workers start out as nurse bees that care for larvae in the nest. Later they embark on foraging trips, specializing in either pollen or nectar collection, and continue to forage until they die. The age when workers initiate foraging and the tendency to collect pollen or nectar have been linked to a rudimentary reproductive physiology in which the protein vitellogenin appears to play a central role. Vitellogenin is normally used to produce egg yolk, but it may affect behavior and lifespan in workers. We tested this hypothesis by knocking down the vitellogenin gene of worker bees. Workers with suppressed vitellogenin levels foraged earlier, preferred nectar, and lived shorter lives. Thus, vitellogenin has multiple effects on honeybee social organization. By using gene knockdown to understand insect social behavior, our study supports the view that social life in bees evolved by co-opting genes involved in reproduction.