Abstract
The receiver sensory system plays a crucial role in the evolution of new communication signals in insects. Among acoustic communicating crickets, the tribe Lebinthini (Eneopterinae) has evolved a unique communication system in that males produce exceptionally high-frequency calls and females respond with vibratory signals to guide males towards them. In this study, we describe nine species of Eneopterinae in which the sound receiving structures have undergone considerable morphological changes. We revealed that the anterior tympanal membrane (ATM) of the ear was extremely thin, as little as 0.35 µm thick, and to the best of our knowledge, this is the thinnest tympanal membrane found in crickets thus far. Measurements of tympanum vibrations obtained from Lebinthus bitaeniatus demonstrated a strong sensitivity towards higher frequencies. The finding also coincides with the neuronal tuning of ascending neurons and the behavioural response of the Lebinthini. The morphologically specialized ATM and its mechanical sensitivity for high frequencies, therefore, may have driven the sensory exploitation of an anti-predator behaviour that led to the evolution of a new communication system known for this group of crickets. The hypothetical phylogenetic origin of the investigated tympanal ears is discussed.
Highlights
Tympanate ears of vertebrates and insects alike allow the detection of pressure changes[1,2]
We demonstrate that the anterior tympanal membrane (ATM) beneath the cuticular fold, subsequently termed the cuticular cap, is extremely thin and its mechanical response is most sensitive to higher sound frequencies
Eneopterinae specimens were obtained from colonies maintained in the laboratory in the Muséum national d’Histoire naturelle (MNHN), representing specimens hatched from eggs or originally collected in Indonesia (Cardiodactylus sumba), Papua New Guinea (Macrobinthus jharnae, Microbinthus pintaudi and Gnominthus baitabagus), Singapore (Nisitrus vittatus), Philippines (Lebinthus sanchezi and L. bitaeniatus) and French Guiana (Eneoptera guyanensis)
Summary
Tympanate ears of vertebrates and insects alike allow the detection of pressure changes[1,2]. Most studies on the functional role of tympanate hearing have been conducted on field crickets (subfamily Gryllinae) of the genera Gryllus and Teleogryllus[7]. In these species, the ear consists of two oval-shaped, translucent membranes, one at the front (the anterior tympanal membrane, ATM) and one at the back of the leg (the posterior tympanal membrane, PTM). In contrast to the obvious anatomical and functional differences of the ATM and PTM in Gryllus and Teleogryllus species, tree crickets (subfamily Oecanthinae) exhibit tympanal membranes (TMs) that are similar in size and thickness, resulting in similar vibration velocities and frequency responses[21]. Benefiting both sexes through reproductive success, this could have led in the Lebinthini to a system in which males generate high-frequency calling songs and females employ a vibrational communication signal[26]
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