Structure, properties and functions of the forewing-hindwing coupling of honeybees.

Worker honeybees (Apis mellifera) are morphologically four-winged, but are functionally dipterous insects. During flight, their fore- and hindwings are coupled by means of the forewing posterior rolled margin (PRM) and hindwing hamuli. Morphological analysis shows that the PRM can be connected to the hamuli, so that the fore- and hindwing are firmly hinged, and can rotate with respect to each other. In the present study, using a combination of scanning electron microscopy (SEM) and confocal laser scanning microscopy (CLSM), we investigate the micromorphology and material composition of the coupling structures on both fore- and hindwings. High-speed filming is utilized to determine the angle variation between the fore- and hindwings in tethered flight. Using sets of two-dimensional (2D) computation fluid dynamic analyses, we further aim to understand the influence of the angle variation on the aerodynamic performance of the coupled wings. The results of the morphological investigations show that both PRM and hamuli are made up of a strongly sclerotized cuticle. The sclerotized hinge-like connection of the coupling structure allows a large angle variation between the wings (135°-235°), so that a change is made from an obtuse angle during the pronation and downstroke to a reflex angle during the supination and upstroke. Our computational results show that in comparison to a model with a rigid coupling hinge, the angle variation of a model having a flexible hinge results in both increased lift and drag with a higher rate of drag increase. This study deepens our understanding of the wing-coupling mechanism and functioning of coupled insect wings.