Marked interspecific differences in the neuroanatomy of the male olfactory system of honey bees (genus Apis)

All honey bee species (genus Apis) display a striking mating behavior with the formation of male (drone) congregations, in which virgin queens mate with many drones. Bees' mating behavior relies on olfactory communication involving queen-but also drone pheromones. To explore the evolution of olfactory communication in Apis, we analyzed the neuroanatomical organization of the antennal lobe (primary olfactory center) in the drones of five species from the three main lineages (open-air nesting species: dwarf honey bees Apis florea and giant honey bees Apis dorsata; cavity-nesting species: Apis mellifera, Apis kochevnikovi, and Apis cerana) and from three populations of A. cerana (Borneo, Thailand, and Japan). In addition to differences in the overall number of morphological units, the glomeruli, our data reveal marked differences in the number and position of macroglomeruli, enlarged units putatively dedicated to sex pheromone processing. Dwarf and giant honey bee species possess two macroglomeruli while cavity-nesting bees present three or four macroglomeruli, suggesting an increase in the complexity of sex communication during evolution in the genus Apis. The three A. cerana populations showed differing absolute numbers of glomeruli but the same three macroglomeruli. Overall, we identified six different macroglomeruli in the genus Apis. One of these (called MGb), which is dedicated to the detection of the major queen compound 9-ODA in A. mellifera, was conserved in all species. We discuss the implications of these results for our understanding of sex communication in honey bees and propose a putative scenario of antennal lobe evolution in the Apis genus.