Vertebrate muscle myosin, the motor protein, has evolved over long periods of time. In the present study, we specifically aimed at identifying how this evolution has fine-tuned myosin conformational states to the specific needs of organisms with different body masses. As myosin has two different relaxed states (super-relaxed and disordered-relaxed), we initially hypothesized that a linear positive correlation would exist between the amount of myosin molecules in the super-relaxed conformation and the body weight of the organisms in which they are expressed. To verify this hypothesis, we extracted muscle fibres from multiple vertebrate species with body weights ranging from grams to tons. By using a loaded Mant-ATP chase protocol, we observed that vertebrate species with body weights above 1000 kilograms have significantly higher proportions of super-relaxed myosin proteins in their muscle fibres. As myosin heads in the super-relaxed conformation consume five times less ATP than the ones in the disordered-relaxed state, our finding suggest that heavy vertebrate animals have adapted their motor protein conformations to potentially avoid inappropriate and large energy consumption in their metabolically demanding muscles.