Fundamental constraints in synchronous muscle limit superfast motor control in vertebrates

Superfast muscles (SFMs) are extremely fast synchronous muscles capable of contraction rates up to 250 Hz, enabling precise motor execution at the millisecond time scale. SFM phenotypes have been discovered in most major vertebrate lineages, but it remains unknown whether all SFMs share excitation-contraction coupling pathway adaptations for speed, and if SFMs arose once, or from independent evolutionary events. Here, we demonstrate that to achieve rapid actomyosin crossbridge kinetics bat and songbird SFM express myosin heavy chain genes that are evolutionarily and ontologically distinct. Furthermore, we show that all known SFMs share multiple functional adaptations that minimize excitation-contraction coupling transduction times. Our results suggest that SFM evolved independently in sound-producing organs in ray-finned fish, birds, and mammals, and that SFM phenotypes operate at a maximum operational speed set by fundamental constraints in synchronous muscle. Consequentially, these constraints set a fundamental limit to the maximum speed of fine motor control.
eLife digest Across animals, different muscle types have evolved to perform vastly different tasks at different speeds. For example, tortoise leg muscles move slowly over several seconds, while the flight muscles of a hummingbird move quickly dozens of times per second. The speed record holders among vertebrates are the so-called superfast muscles, which can move up to 250 times per second. Superfast muscles power the alarming rattle of rattlesnakes, courtship calls in fish, rapid echolocation calls in bats and the elaborate vocal gymnastics of songbirds. Thus these extreme muscles are all around us and are always involved in sound production. Did superfast muscles evolve from a common ancestor? And how do different superfast muscles achieve their extreme behavior? To answer these questions, Mead et al. studied the systems known to limit contraction speed in all currently known superfast muscles found in rattlesnakes, toadfish, bats and songbirds. This revealed that all the muscles share certain specific adaptations that allow superfast contractions. Furthermore, the three fastest examples – toadfish, songbird and bat – have nearly identical maximum speeds. Although this appears to support the idea that the adaptations all evolved from a shared ancestor, Mead et al. found evidence that suggests otherwise. Each of the three superfast muscles are powered by a different motor protein, which argues strongly in favor of the muscles evolving independently. The existence of such similar mechanisms and performance in independently evolved muscles raises the possibility that the fastest contraction rates measured by Mead et al. represent a maximum speed limit for all vertebrate muscles. Any technical failure in a racecar most likely will slow it down, while the same failure in a robustly engineered family car may not be so noticeable. Similarly in superfast muscle many cellular and molecular systems need to perform maximally. Therefore by understanding how these extreme muscles work, we also gain a better understanding of how normal muscles contract.