Neuroanatomy and physiology of the complex tibial organ of an atympanate ensiferan, Ametrus tibialis (Brunner von Wattenwyl, 1888) (Gryllacrididae, Orthoptera) and evolutionary implications.

We investigated the neuroanatomy and physiology of the complex tibial organ of an atympanate ensiferan, the Gryllacridid Ametrus tibialis. This represents the first analysis of internal mechanoceptors in Gryllacridids. The complex tibial organ is tripartite consisting of a subgenual organ, intermediate organ and a homologue organ to the crista acustica of tympanate ensiferan taxa of Tettigoniidae, Haglidae, and Anostostomatidae. The crista homologue contains 23 +/- 2 receptor neurons in the foreleg. It is associated with the leg trachea and found serially in all three thoracic leg pairs. Central projections of the sensory nerve of the complex tibial organ bifurcate in two lobes in the prothoracic ganglion, which do not reach the midline. The axonal endings project into the mVAC, the main vibratory-auditory neuropile of Ensifera. Recordings of the tibial nerve show that the tibial organ is sensitive to vibrational stimuli with a minimum threshold of 0.02 to 0.05 ms(-2) at 200-500 Hz, but rather insensitive to airborne sound. The main function of the tibial organ is therefore vibration sensing, although the specific function of the crista homologue remains unclear. The presence of the crista acustica homologue is interpreted in phylogenetic context. Because ensiferan phylogeny is unresolved, two alternative scenarios can be deduced: (a) the crista homologue is a precursor structure which was co-opted as an auditory system and represent a morphologically highly specialized structure before acquisition of its new function; (b) a previously functional tibial ear is evolutionary reduced but the neuronal structures are maintained. Based on comparison of neuroanatomical details, the crista acustica homologue of A. tibialis could present the neuronal complement of an ear evolutionary precursor structure, which was successively made sensitive to airborne sound by elaboration of cuticular tympana, auditory spiracle and trachea for sound propagation. Copyright 2008 S. Karger AG, Basel.