Embryonic development and evolutionary origin of the orthopteran auditory organs

Abstract

Two different types of ears characterize the order of Orthopteran insects. The auditory organs of grasshoppers and locusts (Caelifera) are located in the first abdominal segment, those of bushcrickets and crickets (Ensifera) are found in the tibiae of the prothoracic legs. Using neuron-specific antibody labelling, we describe the ontogenetic origin of these two types of auditory organs, use comparative developmental studies to identify their segmental homologs, and on the basis of homology postulate their evolutionary origin. In grasshoppers the auditory receptors develop by epithelial invagination of the body wall ectoderm in the first abdominal segment. Subsequently, at least a part of the receptor cells undergo active migration and project their outgrowing axons onto the next anterior intersegmental nerve. During this time the receptor cells and their axons express the cell-cell adhesion molecule, Fasciclin I. Similar cellular and molecular differentiation processes in neighboring segments give rise to serially homologous sensory organs, the pleural chordotonal organs in the pregenital abdominal segments, and the wing-hinge chordotonal organs in the thoracic segments. In more primitive earless grasshoppers pleural chordotonal organs are found in place of auditory organs in the first abdominal segment. In bushcrickets the auditory receptors develop in association with the prothoracic subgenual organ from a common developmental precursor. The auditory receptor neurons in these insects are homologous to identified mechanoreceptors in the meso- and metathoracic legs. The established intra- and interspecies homologies provide insight into the evolution of the auditory organs of Orthopterans.