SYNOPSIS. The function of muscles used to generate force economically and facilitate elastic energy savings in their tendons is compared with muscles that function to produce mechanical power. The underlying architectural design of the muscle and its tendon (if present) dictate much of their functional capacity and role in animal locomotion. Using methods that allow direct recordings of muscle force and fiber length change, the functional design of muscle-tendon systems can now be investigated in vivo. These studies reveal that, in the case of wallaby hindleg muscles, the fibers can maintain sufficient stiffness during tendon stretch and recoil to ensure useful elastic energy recovery and savings of metabolic energy. In the case of the pectoralis muscle of pigeons, although isometric or active lengthening of the muscle's fibers may occur late in the upstroke of the wing beat cycle to enhance force development, the fibers shorten extensively during the downstroke (up to 35% of their resting length) to produce mechanical power for aerodynamic lift and thrust. Oscillatory length change, with force enhancement during active lengthening may be a general feature of muscles that power aerial and aquatic locomotion. Similarly, force enhancement by active lengthening is likely to be important to the design and function of muscles that primarily generate force to minimize energy expenditure/unit force generated, as well as for elastic energy savings within a long tendon. Architectural features of muscle-tendon units for effective elastic energy savings, however, are likely to constrain locomotor performance when mechanical work is required, as when an animal accelerates, either limiting performance or requiring the recruitment of functional agonists with greater mechanical power generating capability (i.e., longer fibers)