Neuroanatomy of the complex tibial organ ofStenopelmatus(Orthoptera: Ensifera: Stenopelmatidae)

Abstract

Stenopelmatidae (or "Jerusalem crickets") belong to the atympanate Ensifera, lacking hearing organs in the foreleg tibiae. Their phylogenetic position is controversial, either as a taxon in Tettigonioidea or within the clade of Gryllacridoidea. Similarly, the origin of tibial auditory systems in Ensifera is controversial. Therefore, we investigated the neuronal structures of the proximal tibiae of Stenopelmatus spec. with the hypothesis that internal sensory structures are similar to those in tympanate Ensifera. In Stenopelmatus the complex tibial organ consists of three neuronal parts: the subgenual organ, the intermediate organ, and a third part with linearly arranged neurons. This tripartite organization is also found in tympanate Ensifera, verifying our hypothesis. The third part of the sense organ found in Stenopelmatus can be regarded by the criterion of position as homologous to auditory receptors of hearing Tettigonioidea. This crista acustica homolog is found serially in all thoracic leg pairs and contains 20 +/- 2 chordotonal neurons in the foreleg. The tibial organ was shown to be responsive to vibration, with a broad threshold of about 0.06 ms(-2) in a frequency range from 100-600 Hz. The central projection of tibial sensory neurons terminates into two equally sized lobes in the primary sensory neuropil, the medial ventral association center. The data are discussed comparatively to those of other Ensifera and mapped phylogenetically onto recently proposed phylogenies for Ensifera. The crista acustica homolog could represent a neuronal rudiment of a secondarily reduced ear, but neuronal features are also consistent with an evolutionary preadaptation.

Laying the foundations of evolutionary and systematic studies in crickets (Insecta, Orthoptera): a multilocus phylogenetic analysis

“…By definition, such a hypothesis cannot be tested by a phylogeny, but it may imply more or less complex patterns of character change according to the phylogenetic topology. Our present phylogeny is parsimoniously consistent with the convergence hypothesis between crickets and mole crickets, and is also consistent with the fact that crickets sensu lato may have structurally diverse acoustic structure (see below); their early acoustic evolution may then not have been straightforward, especially as acoustic communication may have developed in Ensifera within a general framework of communication by vibration and/or sound (Desutter‐Grandcolas, and references therein; Strauss and Lakes‐Harlan, ,b; Stritih and Cokl, ).…”

Mating Behaviour and Vibratory Signalling in Non-Hearing Cave Crickets Reflect Primitive Communication of Ensifera

“…Correspondingly, the construction of the vibratory tibial organs of these species is much more complex than in Rhaphidophoridae [78], since they possess an additional sensory part homologous to the “crista acoustica” of the ensiferan ear [25], [28], [29]. This presumed precursor organ for audition [28] has been proposed to have evolved for enhanced detection of intraspecific vibratory signals, potentially focusing on their high frequency components [25].…”

“…Support for this hypothesis has been provided by the comparative neuroanatomy of the vibration-sensitive tibial organs and their underlying neuronal network in the non-hearing taxa, strongly suggesting these sensory elements as precursors for audition [25], [27], [28], [29]. Based on these results, Rhaphidophoridae are most relevant for research on the presumably ancestral modes of ensiferan communication.…”

Functional Morphology and Evolutionary Diversity of Vibration Receptors in Insects

“…f Central projection of hair sensilla on leg parts, which are somatotopically ordered within the neuropile (two positions are indicated by the two arborization areas). Drawings generalized after for the ganglion outline) [a, b after (Nishino 2000), c after (Strauß and Lakes-Harlan 2008b), e after (Hustert et al 1981) and f after (Mücke and Lakes-Harlan 1995)] aqueous larvae and land-living adults of Plecoptera is rather similar (Wittig 1955), although different mechanical forces might act on the legs.…”

“…Interestingly, the structure of the SGO of (Nishino 2000) or the proximal part in locusts (Field and Pflüger 1989) project into the mVAC; b Other fibers of the FCO have a more lateral projection. c Projection of the midleg CTO of Stenopelmatus (Strauß and Lakes-Harlan 2008b). d Projection of single fiber originating in the SGO.…”