Molecular-scale, nonlinear actomyosin binding dynamics drive population-scale adaptation and evolutionary convergence

TL;DR

This study uses simulations to show how nonlinear actomyosin dynamics influence population adaptation and convergence, revealing the role of mutation rates and resource availability in evolutionary outcomes.

Contribution

It demonstrates how molecular-scale nonlinear actomyosin interactions drive population-level adaptation and convergence over evolutionary timescales, linking biophysical parameters to evolutionary dynamics.

Findings

Populations evolve toward characteristic $oldsymbol{ extalpha^*}$ under resource constraints.

Mutation rate $oldsymbol{ extdelta}$ balances adaptability and robustness.

Intermediate $oldsymbol{ extdelta}$ promotes long-term evolutionary stability.

Abstract

Biological actuators -- from myosin motors to muscles -- follow Hill's model where a dimensionless parameter $\alpha$ captures the nonlinear coupling between contraction rate and force generation. Our prior work identified a characteristic $\alpha^* = 3.85 \pm 2.32$ across natural muscles and showed that $\alpha^*$ optimizes a power-efficiency tradeoff, potentially explaining its prevalence in nature. However, those results reflected short-term actuation tasks whereas phenotypic distributions in $\alpha$ emerge over evolutionary timescales. Here, we use numerical simulations of self-propelled agents to explore how nonlinear actomyosin actuation (parameterized by $\alpha$) shapes population dynamics. Agents of different $\alpha$ compete for resources and reproduce with slight mutations. Without mutations, resource availability drives populations in $\alpha$ toward distinct behaviors: under abundance or scarcity, specialized $\alpha$ survive. However, with mutations and selection, populations evolve toward distributions centered around the characteristic $\alpha^*$ observed in nature. Further, we show that the mutation rate $\delta$ governs a balance between adaptability and robustness: large $\delta$ generates instability and extinction, small $\delta$ prevents feedback, while intermediate $\delta$ enables long-term adaptability while remaining robust to short-term noise. Our results suggest that nonlinear actuation provides a general understanding of energy management in actomyosin systems across a wide range of timescales, ranging from the task-specific to evolutionary. These insights may guide the rational design of active materials with adaptive properties.