Abstract
Weta possess typical Ensifera ears. Each ear comprises three functional parts: two equally sized tympanal membranes, an underlying system of modified tracheal chambers, and the auditory sensory organ, the crista acustica. This organ sits within an enclosed fluid-filled channel–previously presumed to be hemolymph. The role this channel plays in insect hearing is unknown. We discovered that the fluid within the channel is not actually hemolymph, but a medium composed principally of lipid from a new class. Three-dimensional imaging of this lipid channel revealed a previously undescribed tissue structure within the channel, which we refer to as the olivarius organ. Investigations into the function of the olivarius reveal de novo lipid synthesis indicating that it is producing these lipids in situ from acetate. The auditory role of this lipid channel was investigated using Laser Doppler vibrometry of the tympanal membrane, which shows that the displacement of the membrane is significantly increased when the lipid is removed from the auditory system. Neural sensitivity of the system, however, decreased upon removal of the lipid–a surprising result considering that in a typical auditory system both the mechanical and auditory sensitivity are positively correlated. These two results coupled with 3D modelling of the auditory system lead us to hypothesize a model for weta audition, relying strongly on the presence of the lipid channel. This is the first instance of lipids being associated with an auditory system outside of the Odentocete cetaceans, demonstrating convergence for the use of lipids in hearing.
Highlights
Hearing in insects has evolved several times independently [1]
In Tettigoniidae [7], Anostostomatidae [8] and Haglidae [9] the tympanal organs are collectively known as the Complex Tibial Organs (CTOs), which include the subgenual organ, crista acustica, intermediate organ and accessory organ [4,6,10]
Accurate tandem mass analysis of these ions revealed a lipid constituent not corresponding to any hitherto known lipid class (Fig. 1B), indicating that this lipid is likely to be a new category of lipid
Summary
Hearing in insects has evolved several times independently [1]. The frequency sensitivity of these hearing systems tends to correspond to frequencies specific to predator/prey detection and intra-specific communication [1,2,3]. In Tettigoniidae [7], Anostostomatidae [8] and Haglidae [9] the tympanal organs are collectively known as the Complex Tibial Organs (CTOs), which include the subgenual organ, crista acustica, intermediate organ and accessory organ [4,6,10]. These organs sit within a liquid filled channel, that has been presumed to be filled with hemolymph [5,7] – the auditory function of this channel has not been investigated. In some Tettigoniidae species, these adaptations are thought to change the transmission characteristics of the incoming sound wave [7,11,13,14]
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