A precocious adult visual center in the larva defines the unique optic lobe of the split-eyed whirligig beetle Dineutus sublineatus

Introduction: Whirligig beetles (Coleoptera: Gyrinidae) are aquatic insects living on the water surface. They are equipped with four compound eyes, an upper pair viewing above the water surface and a lower submerged pair viewing beneath the water surface, but little is known about how their visual brain centers (optic lobes) are organized to serve such unusual eyes. We show here, for the first time, the peculiar optic lobe organization of the larval and adult whirligig beetle Dineutus sublineatus.Results: The divided compound eyes of adult whirligig beetles supply optic lobes that are split into two halves, an upper half and lower half, comprising an upper and lower lamina, an upper and lower medulla and a bilobed partially split lobula. However, the lobula plate, a neuropil that in flies is known to be involved in mediating stabilized flight, exists only in conjunction with the lower lobe of the lobula. We show that, as in another group of predatory beetle larvae, in the whirligig beetle the aquatic larva precociously develops a lobula plate equipped with wide-field neurons. It is supplied by three larval laminas serving the three dorsal larval stemmata, which are adjacent to the developing upper compound eye.Conclusions: In adult whirligig beetles, dual optic neuropils serve the upper aerial eyes and the lower subaquatic eyes. The exception is the lobula plate. A lobula plate develops precociously in the larva where it is supplied by inputs from three larval stemmata that have a frontal-upper field of view, in which contrasting objects such as prey items trigger a body lunge and mandibular grasp. This precocious lobula plate is lost during pupal metamorphosis, whereas another lobula plate develops normally during metamorphosis and in the adult is associated with the lower eye. The different roles of the upper and lower lobula plates in supporting, respectively, larval predation and adult optokinetic balance are discussed. Precocious development of the upper lobula plate represents convergent evolution of an ambush hunting lifestyle, as exemplified by the terrestrial larvae of tiger beetles (Cicindelinae), in which activation of neurons in their precocious lobula plates, each serving two large larval stemmata, releases reflex body extension and mandibular grasp.