At the Meeting: a Fast and Furious Love Song

Newswise — If you think human romance can be outlandish, welcome to the love life of the plainfin midshipman fish. There are three players, a female who has one shot at laying her eggs under a rock in a shallow bay or estuary somewhere along the Pacific Coast, and two males. Of the males, the big one sings, the little one doesn't. The big one (a.k.a. Type I male) sings in A-flat, or at least he rumbles loudly in the 95-100 Hz range for anywhere from a few seconds to an hour during the mid-summer mating season. The gravid female midshipman follows this 'music' to the Type I male's love nest. Unfortunately for the serenading Type I male, there is often a small, silent, female-impersonating Type II male lurking nearby who darts in uninvited to add his genetic input.

Researchers find this singing, lurking and loving behavior incredibly sexy, scientifically speaking, and midshipman fish are now at the center of high-tech studies by acousticians, evolutionary biologists, neurologists, and cell biologists.

One obvious question was how Type I males manage to hold an A-flat for a full hour. The answer is a 'fast and furious singing muscle', say scientists in the Laboratory of Muscle Biology in the National Institute of Arthritis and Musculoskeletal and Skin Diseases (NIAMS) at NIH. The Type I male midshipman produces his song by a superfast contraction (nearly 6,000 times per minute) of a pair of specialized sonic muscles that vibrate and "drum" the hollow swim bladder to which they attach. In work presented at the American Society for Cell Biology's 43rd Annual Meeting in San Francisco, Kuan Wang, Patrick Nahirney and colleagues say their studies of this superfast fish muscle yielded a radical insight into tissue engineering and a possible model for a human muscle-weakening disease.

The NIAMS researchers used 3D imaging methods to analyze the mechanics, contractile machinery and cytoskeleton of the singing muscle. They found a tissue uniquely adapted for speed and endurance at every level. Inside each cylindrical muscle cell were abundant mitochondria to generate fuel for molecular motors. The motors were (as expected) aligned with actin filaments in long, thin assemblies called myofibrils, and surrounded by membrane 'sacks' that release calcium ions to turn the molecular motors on and off. The first surprise was that the myofibril units were organized radially like wheel spokes to form a hollow, contractile tube. This fan-blade design is radically different from the solid cylinder design of human skeletal and heart muscles. Researchers think that this spoke arrangement ensures speedy delivery of oxygen and fuel, and efficient waste disposal.

The force generated by the spokes is collected and transmitted to specialized attachment sites, called Z-bands, at regular intervals along the myofibrils. Astonishingly, the Z-bands of the Type I male are nearly 50 times thicker than the Z-bands in human muscles.

The contractile cylinder, one in each muscle cell, is surrounded and reinforced mechanically by an elaborate filamentous protein framework. It collects and transmits the force produced by each myofibril to other muscle cells in the sonic muscle tissue. The myofibrils are attached to the framework at the fat Z-bands by a corset-like structure that supports this crucial force transmission and distribution device. This framework also attaches and orchestrates the movement of cell nuclei, mitochondria, and membranes during the fast and furious contraction of the muscle cell.

The roles of the fat Z-bands in singing fish are still mysterious, but Wang and colleagues noted a resemblance to the stiff, rod-like Z-bands characteristic of a human muscle-weakening genetic disease called nemaline myopathy. Thus studies originally aimed at understanding how midshipman fish sing might now throw light on this and other human muscle diseases.

Design and specialization of a superfast, high endurance sound-producing muscle of the midshipman type I male fish, P. C. Nahirney, M.K. Lewis, V. Chen, B.B. Adhikari, K. Wang; Muscle Biology, NIAMS/NIH, Bethesda, MD.