Microscale velocity-dependent unbinding generates a macroscale performance-economy tradeoff in actomyosin systems

Myosin motors are fundamental biological actuators, powering diverse mechanical tasks in eukaryotic cells via ATP hydrolysis. Recent work revealed that myosin’s velocity-dependent detachment rate can bridge actomyosin dynamics to macroscale Hill muscle predictions. However, the influence of this microscale unbinding, which we characterize by a dimensionless parameter α, on macroscale energetic flows—such as power consumption, output and efficiency—remains elusive. Here we develop an analytical model of myosin dynamics that relates nonlinearity α to energetics. Our model agrees with published in-vivo muscle data and, furthermore, uncovers a performance-economy tradeoff governed by α. To experimentally validate this tradeoff, we build HillBot, a robophysical model of Hill’s muscle that mimics nonlinearity. Through HillBot, we decouple α’s concurrent effect on performance and economy, demonstrating that the nonlinearity drives efficiency. We compile 136 published measurements of α in muscle and in mouse myoblasts to reveal a distribution centered at α^* = 3.85 ± 2.32. Synthesizing data from our model and HillBot, we quantitatively show that α^* corresponds to a class of generalist actuators that are both relatively powerful and efficient, suggesting that the performance-economy tradeoff underpins the prevalence of α^* in nature. We leverage these insights and propose a nonlinear variable-impedance protocol to shift along a performance-economy axis in robotic applications.