The evolutionary origin of auditory receptors in Tettigonioidea: the complex tibial organ of Schizodactylidae

Abstract

Audition in insects is of polyphyletic origin. Tympanal ears derived from proprioceptive or vibratory receptor organs, but many questions of the evolution of insect auditory systems are still open. Despite the rather typical bauplan of the insect body, e.g., with a fixed number of segments, tympanal ears evolved at very different places, but only ensiferans have ears at the foreleg tibia, located in the tibial organ. The homology and monophyly of ensiferan ears is controversial, and no precursor organ was unambiguously identified for auditory receptors. The latter can only be identified by comparative study of recent atympanate taxa. These atympanate taxa are poorly investigated. In this paper, we report the neuroanatomy of the tibial organ of Comicus calcaris (Irish 1986), an atympanate Schizodactylid (splay-footed cricket). This representative of a Gondwana relict group has a tripartite sensory organ, homologous to tettigoniid ears. A comparison with morphology-based cladistic phylogeny indicates that the tripartite neuronal organization present in the majority of Tettigonioidea presumably preceded evolution of a hearing sense in the Tettigonioidea. Furthermore, the absence of a tripartite organ in Grylloidea argues against a monophyletic origin and homology of the cricket and katydid ears. The tracheal attachment of sensory neurons typical for ears of Tettigonioidea is present in C. calcaris and may have facilitated cooption for auditory function. The functional auditory organ was presumably formed in evolution by successive non-neural modifications of trachea and tympana. This first investigation of the neuroanatomy of Schizodactylidae suggests a non-auditory chordotonal organ as the precursor for auditory receptors of related tympanate taxa and adds evidence for the phylogenetic position of the group.