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What the buzz was all about: superfast song muscles rattle the tymbals of male periodical cicadas

Patrick C. Nahirney^*, Jeffrey G. Forbes^*, H. Douglas Morris, Susanne C. Chock^* and Kuan Wang^*,1

^* Muscle Proteomics and Nanotechnology Section, Laboratory of Muscle Biology, National Institute of Arthritis and Musculoskeletal and Skin Diseases; and

NIH Magnetic Resonance Imaging Research Facility, National Institute of Neurological Disorder and Stroke, NIH, and Department of Health and Human Services, Bethesda, Maryland, USA

¹Correspondence: Laboratory of Muscle Biology, Bldg. 50, Rm. 1140, National Institute of Arthritis and Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892-8024, USA. E-mail: wangk{at}exchange.nih.gov

Male cicadas produce mating calls by oscillating a pair of superfast tymbal muscles in their anterior abdominal cavity that pull on and buckle stiff-ribbed cuticular tymbal membranes located beneath the folded wings. The functional anatomy and rattling of the tymbal organ in 17 yr periodical cicada, Magicicada cassini (Brood X), were revealed by high-resolution microcomputed tomography, magnetic resonance imaging, electron microscopy, and laser vibrometry to understand the mechanism of sound production in these insects. Each 50 Hz muscle contraction yielded five to six stages of rib buckling in the tymbal, and a small release of muscle tension resulted in a rapid recovery due to the spring-loaded nature of the stiff ribs in the resilin-rich tymbal. The tymbal muscle sarcomeres have thick and thin filaments that are 30% shorter than those in flight muscles, with Z-bands that were thicker and configured into novel perforated hexagonal lattices. Caffeine-treated fibers supercontracted by allowing thick filaments to traverse the Z-band through its open lattice. This superfast sonic muscle illustrates design features, especially the matching hexagonal symmetry of the myofilaments and the perforated Z-band that contribute to high-speed contractions, long endurance, and potentially supercontraction needed for producing enduring mating songs and choruses. —Nahirney, P. C., Forbes, J. G., Morris, H. D., Chock, S. C., Wang, K. What the buzz was all about: Superfast song muscles rattle the tymbals of male periodical cicadas.

Key Words: multimodal imaging • Z-band lattice • myofilament length regulation • sarcomere proportion • supercontraction