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

Abstract

IntroductionWhirligig 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.ResultsThe 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.ConclusionsIn 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.

Genealogical correspondence of a forebrain centre implies an executive brain in the protostome–deuterostome bilaterian ancestor

“…odontocete whales [64,65]. Another trait is that the location of any centre that is claimed to genealogically correspond to an insect mushroom body is situated in the most anterior neuromere of the brain or just the rostral brain in those invertebrates that possess asegmental brains, such as nemertean worms, annelids and Platyhelminthes.…”

“…These send parallel tracts of axons through the cornu ammonis that form an orthogonal matrix, interfacing with local interneurons, afferent inputs from the entorhinal cortex, and projecting to the subiculum and back to the entorhinal cortex [63]. Another trait is that centres morphologically corresponding to mushroom bodies are, at least ancestrally, supplied from primary olfactory centres except in species where there has been an evolved switch of modality or loss of odorant receptors, as in some anosmic insects and odontocete whales [64,65]. Another trait is that the location of any centre that is claimed to genealogically correspond to an insect mushroom body is situated in the most anterior neuromere of the brain or just the rostral brain in those invertebrates that possess asegmental brains, such as nemertean worms, annelids and Platyhelminthes.…”

Under- and over-water halves of Gyrinidae beetle eyes harbor different corneal nanocoatings providing adaptation to the water and air environments

“…However, optical properties of the air and the water are different, so one could expect a difference in the overwater and underwater eye anatomy in whirligig beetles. Although recent studies have revealed a peculiar way of organization of the visual brain centers in Gyrinidae to accommodate the split eye vision of these insects4, the overall morphology and organization of the two eye portions is remarkably similar56. This suggests that finer aspects of the over- and under-water eyes of whirligig beetles, escaping previous analyses, may be present to accommodate the different optical requirements.…”

Crustacean Larvae—Vision in the Plankton

“…After larval-adult metamorphosis, the larval eye and its visual neuropils completely degenerate and are replaced by the adult system. This transition is comparable to what occurs in holometabolous insects, where the adult compound eyes and the four underlying visual neuropils form de novo from specialized eye-antennal imaginal discs and replace the larval visual system after metamorphosis (Fischbach and Hiesinger 2008;Lin and Strausfeld 2013;Sbita et al 2007).…”