Some praying mantids have sensitive ultrasonic hearing arising from a unique 'cyclopean' ear located in the ventral metathorax. The present study explores the evolutionary history of the mantis auditory system by integrating large anatomical, neurophysiological, behavioural, and molecular databases. Using an 'auditory phylogeny' based on 13 morphological characters, we identified a primitively earless form of metathoracic anatomy in several extant taxa. In addition, there are five distinct mantis auditory systems. Three of these can be identified anatomically, and the other two can only be detected neurophysiologically. Superimposing these results onto a phylogenetic tree derived from molecular data from seven genes shows that the cyclopean mantis ear evolved once approximately 120 Mya. All the other auditory system types are either varying degrees of secondary loss, or are recent innovations that each occurred independently multiple times. The neurophysiological response to ultrasound is remarkably consistent across all taxa tested, as is the multicomponent, in-flight behaviour triggered by ultrasound. Thus, mantids have an ancient, highly conserved auditory neural-behavioural system. Although ultrasonic hearing in several insect groups evolved in response to bat predation, mantis hearing predates the appearance of bats (approximately 63 Mya) and must originally have functioned in communication, prey detection, or avoidance of nonbat predators.
The totally aquatic pipid frog Xenopus borealis produces long trains of click‐like sound at high sound pressure levels (> 105 dB SPL) underwater at night. While X. borealis retains an essentially terrestrial respiratory tract, the larynx is highly modified in two ways. First, the cricoid cartilage is greatly expanded posteriorly to form a large ‘box’. Portions of this cricoid box are composed of an unusual elastic cartilage. Second, portions of the arytenoid cartilages are elaborated into calcified rods with disc‐like enlargements at their posterior ends. These discs are the only freely moveable components within the larynx–there are no vocal cords. Artificial stimulation of a pair of muscles controlling the discs and discrete lesions that impair their movement demonstrate that motion of the discs is both necessary and sufficient for click production. Unlike all other anurans, X borealis does not use a moving air column in sound production. A possible mechanism of click production involves two steps: (1) at first, the discs are held tighdy apposed in the midline by fluid adhesive forces, and contraction of bipennate muscles is isometric; (2) when the muscle tension exceeds the adhesive force, the discs separate with very high acceleration leaving a vacuum between them. Air rushing into the space at high speed (an implosion) produces the click. The cricoid box shapes the frequency spectrum of the clicks, and opening the box broadens the power spectrum. The power spectrum of clicks produced by males after breathing helium is unchanged.
Sexual dimorphism of tympanate auditory systems in insects has bees described in only a few taxonomically isolated cases. However, widespread sexual dimorphism occurs in the ultrasound‐sensitive, midline ear of the praying mantis.
In dimorphic species, it is always the female mantis that shows a reduction in ultrasonic hearing. The dimorphism may be mild—a difference in tuning and small reduction in sensitivity—or extreme with no evidence of audition in the female. In all but the mildest cases, the reduction in hearing is accompanied by significant anatomical divergence from the male ear structure. Two distinct metathoracic groove (‘ear’) types are linked to hearing reduction in the females.
Anatomical evidence of auditory sexual dimorphism appears in 34% of the 183 mantis genera examined. The dimorphic genera are widely but non‐uniformly distributed within three of the four largest mantis families.
Auditory sexual dimorphism is closely correlated with dimorphism in wing length. In general, mantises with functional wings have sensitive ultrasonic hearing while those with short wings do not. These findings support the hypothesis that ultrasonic hearing in mantises is part of a defensive system against attack by echolocating bats.
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