Evolutionary transition from stretch to hearing organs in ancient grasshoppers

Abstract

Ears of modern insects occur on a wide variety of body parts and are thought to have evolved from ubiquitous stretch or vibration receptors1,2,3,4. This relationship, based on comparative anatomy and similarities in the embryological development of ears in divergent taxa5,6,7, has led to the widespread assumption of homology of these structures in insects, although this has not been tested rigorously. Here we report on the hearing organs of a relatively ancient8, atympanate bladder grasshopper9,10,11 (Bullacris membracioides), which is capable of signalling acoustically over 2 km12. We show that, within single individuals of this species, serially repeated abdominal ears show functional continuity from simple to more complex forms. All 12 morphologically differentiated organs respond to sound frequencies and intensities that are biologically significant, and mediate adaptive behavioural responses. By linking observations at the anatomical, physiological and behavioural level, our experiments provide evidence for the transition in function and selective advantage during the evolutionary development of this complex structure13,14. It is possible that ancestral insects with only simple pleural receptors had auditory capability covering distances substantially greater than contemporary insects with tympanate ears.

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Figure 1: Chordotonal organs in abdominal segments A1–A6 of adult bladder grasshoppers are differentiated morphologically, exhibiting two levels of complexity.
Figure 2: Six pairs of abdominal chordotonal organs in adult pneumorids respond to sound with action-potential discharges at frequencies and intensities that are biologically significant.
Figure 3: Chordotonal organs mediate adaptive behavioural responses to acoustic signals.

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Acknowledgements

We thank the Alexander family, B.-A. Gereben-Krenn, M. Rieser, H. Schuster, W.vanStaaden and R. Wright for assistance; A. Delago for help with experiments; C. Kernbichler, S. Ott, K.Steiner and Wirsam Scientific & Precision Equipment for technical assistance; the KwaZulu/Natal Parks Board for collecting permits; and G. Boyan, J. Fullard, R. Huber and D. Robert for comments. This research was supported by the Austrian Science Foundation.

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Correspondence to Moira J. van Staaden.

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van Staaden, M., Römer, H. Evolutionary transition from stretch to hearing organs in ancient grasshoppers. Nature 394, 773–776 (1998). https://doi.org/10.1038/29517

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