Neurometamorphosis of the ear in the gypsy moth, Lymantria dispar, and its homologue in the earless forest tent caterpillar moth, Malacosoma disstria

The adult gypsy moth, Lymantria dispar (Lymantriidae: Noctuoidea) has a pair of metathoracic tympanic ears that each contain a two-celled auditory chordotonal organ (CO). The earless forest tent caterpillar moth, Malacosoma disstria (Lasiocampidae: Bombycoidea), has a homologous pair of three-celled, nonauditory hindwing COs in their place. The purpose of our study was to determine whether the adult CO in both species arises from a preexisting larval organ or if it develops as a novel structure during metamorphosis. We describe the larval metathoracic nervous system of L. dispar and M. disstria, and identify a three-celled chordotonal organ in the anatomically homologous site as the adult CO. If the larval CO is severed from the homologue of the adult auditory nerve (IIIN1b1) in L. dispar prior to metamorphosis, the adult develops an ear lacking an auditory organ. Axonal backfills of the larval IIIN1b1 nerve in both species reveal three chordotonal sensory neurons and one nonchordotonal multipolar cell. The axons of these cells project into tracts of the central nervous system putatively homologous with those of the auditory pathway in adult L. dispar. Following metamorphosis, M. disstria moths retain all four cells (three CO and one multipolar) while L. dispar adults possess two cells that service the auditory CO and one nonauditory, multipolar cell. We conclude that the larval IIIN1b1 CO is the precursor of both the auditory organ in L. dispar and the putative proprioceptor CO in M. disstria and represents the premetamorphic condition of these insects. The implications of our results in understanding the evolution of the ear in the Lepidoptera and insects in general are discussed.