Phenotypic deconstruction reveals involvement of manganese transporter malvolio in honey bee division of labor

Molecular analysis of a complex behavioral phenotype is facilitated by dissecting it into simpler behavioral components. Using this approach, we present evidence implicating increased manganese transport by the malvolio (mvl) gene into brain cells as one factor that influences age-related division of labor in honey bee colonies. We studied mvl because manganese affects sucrose responsiveness in Drosophila melanogaster, and sucrose responsiveness is related to division of labor in honey bee colonies. Honey bee foragers are more responsive to sucrose in the laboratory than are younger nurse bees, and pollen foragers are more responsive to sucrose than nectar foragers. Levels of mvl mRNA in the brain and manganese in the head were higher in pollen foragers compared with nurses, with nectar foragers intermediate. Manganese treatment increased honey bee sucrose responsiveness and caused precocious foraging. Manganese levels showed a similar pattern to mvl mRNA but manganese treatment did not increase pollen foraging. These results suggest that, while there are molecular pathways common to sucrose responsiveness and division of labor, linkages between a complex behavior and some of its simpler behavioral components are not obligatory. Together with previous findings, these results support the idea that some feeding-related genes in Drosophila have been used in social evolution to regulate division of labor.