Juvenile-hormone-dependent interaction of actin and spectrin is crucial for polymorphic differentiation of the larval honey bee ovary.

Programmed cell death in the worker ovary of Apis mellifera reduces the number of ovarioles during metamorphosis from 150-200 primordia to less than 10. In contrast, practically all ovarioles in the ovary of queens survive to the adult stage. The correct formation and persistence of polyfusomes has been suggested as a critical factor for ovariole survival. We have analyzed the developmental dynamics of F-actin and alpha-spectrin in fusomes of queen and worker larvae, and in juvenile-hormone-treated worker larvae. Small fusomes containing actin and spectrin can be detected in the ovaries of fourth instar larvae in both castes. After molting to the fifth instar, the actin-spectrin association persists in the enlarged fusomes of queen ovarioles. In workers, actin dissociates from the fusomal and cortical alpha-spectrin. Coinciding with the appearance of apoptosis markers, large agglomerates of actin are detectable in worker ovarioles. Treatment of fourth-instar worker larvae with juvenile hormone rescues ovarioles from apoptosis and maintains the actin-spectrin association. Juvenile-hormone-dependent actin-spectrin interaction is thus one of the earliest steps in the differentiation of a polymorphic ovary. Plasticity in ovariole numbers as a result of hormone-dependent fusome formation may be a more widespread phenomenon in insects, extending beyond caste polymorphism in highly eusocial Hymenoptera.