What determines the number of auditory sensilla in the tympanal hearing organs of Tettigoniidae? Perspectives from comparative neuroanatomy and evolutionary forces

Abstract

Insects have evolved complex receptor organs for the major sensory modalities. For the sense of hearing, the tympanal organ of Tettigoniidae (bush crickets or katydids) shows remarkable convergence to vertebrate hearing by impedance conversion and tonotopic frequency analysis. The main auditory receptors are scolopidial sensilla in the crista acustica. Morphological studies established that the numbers of auditory sensilla are species-specific. However, the factors determining the specific number of auditory sensilla are not well understood. This review provides an overview of the functional organization of the auditory organ in Tettigoniidae, including the diversification of the crista acustica sensilla, a list of species with the numbers of auditory sensilla, and a discussion of evolutionary forces affecting the number of sensilla in the crista acustica and their sensitivity. While all species of Tettigoniidae studied so far have a crista acustica, the number of sensilla varies on average from 15–116. While the relative differences or divergence in sensillum numbers may be explained by adaptive or regressive changes, it is more difficult to explain a specific number of sensilla in the crista acustica of a specific species (like for the model species Ancistrura nigrovittata, Copiphora gorgonensis, Gampsocleis gratiosa, Mecopoda elongata, Requena verticalis, or Tettigonia viridissima): sexual and natural selection as well as allometric relationships have been identified as key factors influencing the number of sensilla. Sexual selection affects the number of auditory sensilla in the crista acustica by the communication system and call patterns. Further, positive allometric relationships indicate positive selection for certain traits. Loss of selection leads to evolutionary regression of the auditory system and reduced number of auditory sensilla. This diversity in the auditory sensilla can be best addressed by comparative studies reconstructing adaptive or regressive changes in the crista acustica.

Comparative micromechanics of bushcricket ears with and without a specialized auditory fovea region in the crista acustica

“…Bushcricket ears are often specialized to match habitat conditions and specific behavioural tasks, whether it is to avoid predators by acoustic detection [54] or for intraspecific communication [55,56]. Duetting bushcrickets, like A. fenestrata, have more scolopidial units in their respective hearings organs in general, compared to sister species with other mate-finding strategies [57].…”

Reconstruction of sound driven, actively amplified and spontaneous motions within the tree cricket auditory organ

“…In katydids, the auditory organ is known as the crista acustica (Montealegre-Z. et al, 2012) and has a similar structure with one crucial difference, the mechanosensory neurons are not attached to the wall of the auditory vesicle (Strauß, 2019). In fact, phylogenetic evidence suggests that the two organs evolved independently from a precursor intermediate organ (Song et al, 2020;Strauß and Lakes-Harlan, 2014).…”

Auditory tuning in the bushcricket miniature hearing organ

“…Female bushcrickets, the males’ intended audience, have to perform essentially the same feat but with miniature hearing organs located not on the head but on the upper tibia of the forelegs. These ears are typically only around 1 to 2 mm in size and contain rarely more than 100 neurons ( 3 ). Nevertheless, these tiny insect ears share a surprising amount of structural and functional similarities with our ears, some of which Vavakou et al ( 4 ) uncover.…”

“…This organ is located along the proximal–distal length of the dorsal wall (DW) and consists of a row of neurons with their sensory dendrites covered in cap cells (CCs), which are linked with an overlying tectorial membrane (TM), covered by a fluid-filled channel ( Fig. 1 ) ( 3 ). Analogous to the mammalian inner ear, the morphology of the CA changes gradually along its length, exhibiting, amongst others, decreasing CC sizes and DW and TM width from proximal start to distal end ( 7 ).…”

“…Analogous to the mammalian inner ear, the morphology of the CA changes gradually along its length, exhibiting, amongst others, decreasing CC sizes and DW and TM width from proximal start to distal end ( 7 ). These size variations cause changes in mass, stiffness, and resonance of the CA and are the basis for a tonotopical activation of the sensory neurons along the CA via mechanical traveling waves ( 3 , 7 – 9 ). This generates a frequency-place map, with the location of neurons activated by an acoustic signal depending on the signal’s frequency ( 10 , 11 ).…”