Visual Specializations in the Brain of the Split-Eyed Whirligig Beetle Dineutus sublineatus

Abstract

Whirligig beetles are gregarious aquatic insects living on the water surface. They are equipped with two separate pairs of compound eyes, an upper aerial pair and a lower aquatic pair, but little is known about how their brains are organized to serve such an unusual arrangement. In the first study of this dissertation, I describe the neural organization of their primary visual centers (the optic lobes) of the larval and adult whirligig beetle Dineutus sublineatus. I show that the divided compound eyes of adult beetles supply elaborate optic lobes in the brain that are also split into an upper and a lower half, each optic lobe comprising an upper and lower lamina, an upper and lower medulla, and a partly split bilobed lobula. The exception is the fourth neuropil, the lobula plate. Studies of their development show that the lobula plate Anlagen serving the upper and lower eyes develop at different rates and thus different developmental stages. The upper lobula plate develops precociously in the larva and is thought to process information that enables subaquatic ambush hunting. During metamorphosis the upper lobula plate degenerates and is lost as are the larval stemmatal eyes supplying it. The lower lobula plate develops later, during metamorphosis, and is present in the imago where it is supplied by the lower compound retina. By analogy with dipteran lobula plates it is proposed to support subaquatic locomotory balance. In the subsequent study, I describe the neural organization of the whirligig beetle’s mushroom bodies, a pair of prominent brain centers in the forebrain that are best known for their roles in higher olfactory processing and olfactory-based learning and memory. I found that unlike other insects examined so far, the calyces of the whirligig beetle’s mushroom bodies are exclusively supplied by visual neurons from optic lobe neuropils serving the pair of upper aerial compound eyes, thereby showing a complete modality switch from olfaction to vision in this brain center. These findings, along with multiple evidence from hymenopteran insects and cockroaches, suggest that insect mushroom bodies are not merely olfactory-related but may be involved in visual tasks, such as memory of place. In the last study, I describe experiments to demonstrate that a group of D. sublineatus is able to learn their location with respect to visual cues provided from above the water line, and simultaneously establish and maintain their relative positions with each other within the group. These results provide an explanation as to how a collective, such as several hundred whirligig beetles, can maintain cohesion and remember landmarks that "anchor" the collective at a particular location in a pond or stream. Using techniques in comparative neuroanatomy, this dissertation documents visual specializations of an insect brain that has evolved to suit a unique group-living lifestyle on the water surface. In addition, the spatial learning paradigm described in the third study provides an essential assay for future lesion studies to determine if mushroom bodies are indeed required for visually mediated spatial learning and memory.