Evolutionary adaptation of contractile performance in muscle of ectothermic winter-flying moths

Abstract

The temperature-sensitivity of muscle performance in a winter-flying ecotothermic moth (Operophtera bruceata) was examined and compared with that of a summer-flying endothermic hawkmoth (Manduca sexta). O. bruceata muscle contracted over a temperature range of 1­28 °C, whereas M. sexta muscle contracted at temperatures of 13­42.5 °C. Maximum (unloaded) contraction velocity (Vmax) was greater in O. bruceata over most of the range of temperatures where muscle from both species was excitable (3­4 lengths s-1 versus 0.6­3.6 lengths s-1 at 13­28 °C), but M. sexta muscle achieved a much higher Vmax at the temperature that this species maintains during flight (10 lengths s-1 at 40­42.5 °C). The capacity of O. bruceata muscle to generate tension was approximately twice that of M. sexta muscle (peak tetanic tension of 13.9 versus 7.0 N cm-2). This greater force-generating capacity in O. bruceata largely offset its lower shortening velocity, such that maximum instantaneous power output was equivalent in both species at temperatures below 35 °C (approximately 100­120 W kg-1). M. sexta muscle achieved instantaneous power outputs of up to 202 W kg-1 at temperatures of 40­42.5 °C. Muscle activation and deactivation (measured by times to peak tension and to half-relaxation during isometric twitches) were most rapid for O. bruceata at temperatures of 15­30 °C and for M. sexta at temperatures of 30­40 °C. Data for power output of flight muscle from these moths are combined with estimates of induced power required for flight in order to show how adaptations for thermal sensitivity of muscle power output interact with morphology (low wing-loading, high flight muscle ratio) to allow O. bruceata moths to fly at extremely low body temperatures, and to construct a model showing how the fecundity of flightless O. bruceata females would decline if they were to regain the ability to fly. Marginal flight over a narrow range of temperatures for O. bruceata females would require a 17 % reduction in fecundity; to fly over as large a range of temperatures as do males would require an 82 % reduction in fecundity.