Abstract
In orthopteran insects, a complex tibial organ has evolved to detect substrate vibrations and/or airborne sound. Species of New Zealand weta (Anostostomatidae) with tympanal ears on the foreleg tibia use this organ to communicate by sound, while in atympanate species (which communicate by substrate drumming) the organ is unstudied. We investigated the complex tibial organ of the atympanate ground weta, Hemiandrus pallitarsis, for vibration detection adaptations. This system contains four sensory components (subgenual organ, intermediate organ, crista acustica homolog, accessory organ) in all legs, together with up to 90 scolopidial sensilla. Microcomputed tomography shows that the subgenual organ spans the hemolymph channel, with attachments suggesting that hemolymph oscillations displace the organ in a hinged-plate fashion. Subgenual sensilla are likely excited by substrate oscillations transmitted within the leg. Instead of the usual suspension within the middle of the tibial cavity, we show that the intermediate organ and crista acustica homolog comprise a cellular mass broadly attached to the anterior tibial wall. They likely detect cuticular vibrations, and not airborne sound. This atympanate complex tibial organ shows elaborate structural changes suggesting detection of vibrational stimuli by parallel input pathways, thus correlating well with the burrowing lifestyle and communication by substrate-transmitted vibration.
Highlights
Different groups of orthopteran insects, including grasshoppers (Caelifera), crickets, tettigoniids and weta (Ensifera), have evolved diverse and complex signalling systems based on the production and reception of sound or substrate vibration[1,2,3,4,5]
The complex tibial organs of tree weta (Hemideina spp.) have been studied in detail, where they consist of the subgenual organ (SGO), intermediate organ (IO), and the crista acustica (CA) together with an accessory organ (AO)[20, 25, 27, 28]
The SGO is an important detector for substrate vibrations[16, 17, 26, 29], while the sensilla of the CA are associated with the cuticular tympana and are the main detectors for airborne sound[25, 28, 30]
Summary
Different groups of orthopteran insects, including grasshoppers (Caelifera), crickets, tettigoniids and weta (Ensifera), have evolved diverse and complex signalling systems based on the production and reception of sound or substrate vibration[1,2,3,4,5]. The neuroanatomical organisation of the complex tibial organ in the tree weta closely resembles that of the tympanate Tettigoniidae[26, 31] and Prophalangopsidae (Cyphoderris)[32], the organ has not been studied in the atympanate ground weta species This raises questions concerning sensory evolution: is the complex tibial organ conserved in evolution, how is it modified by adaptations to different stimuli, and has the prolonged isolation of New Zealand led to differences in the mechanosensors compared to other Ensifera?. The New Zealand weta fauna allows for a comparative investigation of these sensory structures between closely related species of the tympanate tree weta Hemideina and the atympanate ground weta Hemiandrus. For the first time, distinct attachments of the atympanate mechanosensory organs which provide parallel input pathways for vibration stimuli
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