Temperature gradients drive mechanical energy gradients in the flight muscle of Manduca sexta

Abstract

A temperature gradient throughout the dominant flight muscle (dorsolongitudinal muscle, DLM(1)) of the hawkmoth Manduca sexta, together with temperature-dependent muscle contractile rates, demonstrates that significant spatial variation in power production is possible within a single muscle. Using in situ work-loop analyses under varying muscle temperatures and phases of activation, we show that regional differences in muscle temperature will induce a spatial gradient in the mechanical power output throughout the DLM(1). Indeed, we note that this power gradient spans from positive to negative values across the predicted temperature range. Warm ventral subunits produce positive power at their in vivo operating temperatures, and therefore act as motors. Concurrently, as muscle temperature decreases dorsally, the subunits produce approximately zero mechanical power output, acting as an elastic energy storage source, and negative power output, behaving as a damper. Adjusting the phase of activation further influences the temperature sensitivity of power output, significantly affecting the mechanical power output gradient that is expressed. Additionally, the separate subregions of the DLM(1) did not appear to employ significant physiological compensation for the temperature-induced differences in power output. Thus, although the components of a muscle are commonly thought to operate uniformly, a significant within-muscle temperature gradient has the potential to induce a mechanical power gradient, whereby subunits within a muscle operate with separate and distinct functional roles.