Ideal For Booming Mating Calls, Certain Fish Muscles Have Evolved So Fully That They're Unfit For Much Else

The finding, made in studies of the toadfish Opsanus tau, is the cover story in the Oct. 7 issue of the journal Proceedings of the Royal Society. It’s the first demonstration of different skeletal muscles in the same species diverging so thoroughly through evolution that they’re now mutually exclusive.

In the case of the toadfish, the split is primarily on the basis of the speed at which the muscle contracts, with "superfast" skeletal muscle for the mating call and slower skeletal muscle to handle swimming and other movements. Unlike the skeletal muscle found in most species, the two types are apparently not interchangeable: ounce for ounce, the fleet but feeble superfast muscle can generate just 5 to 15 percent the power of the fish’s other muscles.

"This is an excellent example of tradeoffs in biological design," said lead author Lawrence C. Rome, a professor of biology at Penn. "No biological system can do everything; when you tune a system for one function, you almost necessarily reduce its ability to perform another function. What makes this particular case so striking is that the molecular modifications have gone so far to increase speed that the muscle has become completely unable to perform other functions such as locomotion."

A generally sluggish resident of shallow, murky waterways from Massachusetts to Florida, the homely toadfish is distinguished primarily by the superfast muscles surrounding an organ called a swimbladder, which it uses to create its mating call. These muscles are the fastest known among vertebrates, contracting and relaxing as many as 200 times a second, five times as rapid as the beating of a hummingbird’s wings and 50 times faster than any sprinter’s legs.

But this swimbladder muscle, which has evolved to be fast above all else, exerts virtually no physical force. Indeed, Rome and co-author Iain S. Young determined that to generate the same power as the toadfish’s ordinary locomotive muscle, swimbladder muscle equivalent to three times the toadfish’s volume would be required.

"Although we showed more than a decade ago that fish slow muscle can’t do the job of fast muscle, it was generally assumed that fast muscle could always do the job of slow muscle," Rome said. "This is the first study to show that superfast muscle is unable to do the job of slower muscle and thus that the designs are mutually exclusive."

Humans don’t have anything as fast as the toadfish’s swimbladder muscles, but our eye muscles are thought to operate at high speeds. There is some evidence, Rome said, that like swimbladder muscles, eye muscles generate lower forces than locomotory muscles and could possibly be considered mutually exclusive as well.

Toadfish live in shallow estuaries where visibility is poor, but sound carries very well. The male toadfish uses its mating call to lure females to nests in discarded coffee cans, around pilings or excavated out of the marsh. On Cape Cod, where Rome conducted his research, the call of the male toadfish can be heard ­-- in many cases even above water, amplified by metal or fiberglass boat hulls --­ from late April through July.

Rome and Young’s work, conducted in part at the Marine Biological Laboratories in Woods Hole, Mass., was supported by the National Science Foundation and the National Institutes of Health.