Main

In Drosophila melanogaster, the antennae mediate the detection of conspecific 'love songs'5,6. Anatomically, each antenna is an asymmetric structure consisting of three segments and a feather-like arista3 (Fig. 1a). Laser vibrometric analysis of sound-induced vibrations7 reveals that the arista and the club-shaped third segment together constitute a mechanical entity — the sound receiver. Both antennal parts oscillate sympathetically in response to acoustic stimulation, consistently exhibiting a moderately damped resonance at 426 ± 16 Hz (quality factor, Q = 1.2 ± 0.1; 8 flies; Fig. 1b).

Figure 1: Anatomy, mechanical response and operational mode of Drosophila antennal hearing organs.
figure 1

a, Anatomy. Left panel, scanning electron micrograph showing the three antennal segments (numbered) and the arista; right panel, longitudinal section through segments 2 and 3. Scale bars, 100 μm. b, Mechanical response to acoustic random-noise stimulation. The arista and the third segment exhibit identical resonance characteristics and rotate about the longitudinal axis of the latter. Frequency spectra show the magnitude and phase of the vibration velocity (measured by microscanning laser Doppler vibrometry7) normalized to the particle velocity in the sound field (measured by a particle-velocity microphone at the antenna's position7). A response magnitude of unity indicates equal vibration velocity and particle velocity, and a phase of + 90° means that the vibration velocity leads the particle velocity by one-quarter of an oscillation cycle. The acoustic stimulus (mean particle velocity ± 0.04 mm s−1) induced maximal displacements of ± 20 nm and rotation of ± 0.003°. Insets, measurement sites and colour convention (drawing by P. Bryant10). c, Operational mode, showing analogy between antennal mechanics and a rotating key. Yellow arrows, input force; blue arrows, rotation; red arrows, output force.

Full size image

Mechanical measurements at different locations (Fig. 1b) show that the entire arista oscillates as a stiff rod, with its vibration velocity continuously decreasing from tip to base. Remarkably, this oscillation is accompanied by rotation of the third segment. The 180° phase shift between the mechanical responses of opposite edges (Fig. 1b) unambiguously shows that they move in opposite directions and that this segment rotates about its longitudinal axis. This rotation is a direct consequence of the radial orientation of the arista, which breaks mechanical symmetry. Physically, the arista introduces a moment arm, increases the effective surface area, and thus determines the twisting force (torque) exerted by sound.

When stimulated acoustically, the third segment rotates like the bow of a key (Fig. 1c). Moreover, the proximal part of this segment presents a stalk that fits into a pit in the second segment, like a key in its lock. Extending along the rotational axis, this stalk transmits the rotation 'downstream', like a key's stem (Fig. 1a, c). Before connecting to the second segment, the stalk bends, forming a hook. This hook then oscillates like a key's bit (Fig. 1a, c). This vibration will maximally stretch and compress the auditory receptors which, notably, are attached perpendicularly to both sides of the hook.

Unlike other animals, Drosophila makes use of sound-induced rotation to channel acoustic energy to its auditory receptor neurons — it has 'rotational ears'. This unconventional mechanism relies on a simple trick: the hook balances the asymmetry introduced by the arista, thereby guaranteeing a receptor activation that compares to that in other insect auditory systems8. The third segment of the Drosophila antenna is also the primary organ of olfaction and carries hundreds of olfactory sensilla9. As hearing relies on rotation, the two sensory modalities can co-exist without compromising their respective functions. Such an evolutionary solution is elegant; flies did not turn their nose into an ear, they turn their nose to hear.