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Abstract
SummarySubstrate-borne vibratory signals are thought to be one of the most ancient and taxonomically widespread communication signals among animal species, including Drosophila flies.1, 2, 3, 4, 5, 6, 7, 8, 9 During courtship, the male Drosophila abdomen tremulates (as defined in Busnel et al.10) to generate vibrations in the courting substrate.8,9 These vibrations coincide with nearby females becoming immobile, a behavior that facilitates mounting and copulation.8,11, 12, 13 It was unknown how the Drosophila female detects these substrate-borne vibratory signals. Here, we confirm that the immobility response of the female to the tremulations is not dependent on any air-borne cue. We show that substrate-borne communication is used by wild Drosophila and that the vibrations propagate through those natural substrates (e.g., fruits) where flies feed and court. We examine transmission of the signals through a variety of substrates and describe how each of these substrates modifies the vibratory signal during propagation and affects the female response. Moreover, we identify the main sensory structures and neurons that receive the vibrations in the female legs, as well as the mechanically gated ion channels Nanchung and Piezo (but not Trpγ) that mediate sensitivity to the vibrations. Together, our results show that Drosophila flies, like many other arthropods, use substrate-borne communication as a natural means of communication, strengthening the idea that this mode of signal transfer is heavily used and reliable in the wild.3,4,7 Our findings also reveal the cellular and molecular mechanisms underlying the vibration-sensing modality necessary for this communication.
Highlights
Drosophila melanogaster wild flies exhibit substrateborne communication signals similar to laboratory fly stocks Substrate-borne vibratory signals during courtship have been reported in D. melanogaster laboratory stocks,[8,9,11] but not in wild D. melanogaster
The durations of the interpulse intervals (IPIs) are often used by animals for signal recognition;[1,4,7,14,15,16,17,18,19] we used laser vibrometry to measure and compare the IPI of the substrate-borne vibrations produced by wild and laboratory male’s abdominal tremulations and found them to be similar to one another (Figure S1D)
D. melanogaster courtship relies on a near-field air-borne signal, the ‘‘love song,’’ which is produced by the male’s wing fluttering.[21,22,23,24,25,26,27,28]
Summary
Nutritional, and receptive status of the female.[21,23] Chemical, visual, and air-borne signals modify the behavior of the male and the responsiveness of the female.[21,22,23,24,25,26,27,28,29,30] D. melanogaster courtship relies on a near-field air-borne signal, the ‘‘love song,’’ which is produced by the male’s wing fluttering.[21,22,23,24,25,26,27,28] We surgically removed the whole antennae or only the aristae (essential for air-borne sound reception)[26] from females, paired them with normal males, studied their courtship, and compared it with the courtship of intact Oregon-R couples (Figures 1A–1C, S1C, and S1E). Female immobility strongly coincided with bouts of male tremulation (Figure 1B), and female immobility was low when the male did not tremulate (Figures 1B and 1C; Table S1). These data are consistent with the hypotheses that female immobility is not regulated by air-borne signals and that females do not detect males’ tremulations via air-borne signals
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