An integrated approach towards characterising the functional mechanics and energetics of insect fight muscles

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Insects are the most diverse and economically important classes of animals on earth and there is little doubt that one of the reasons for their great success is their incredible flying ability, which typically far surpasses that of vertebrates in terms of manoeuvrability and control. In the time that it takes a human to blink, a blowfly can beat its wings 50 times, powering and controlling each wingbeat using numerous tiny muscles - some as thin as a human hair. Unlike their flying verterbrate counterparts, insect wings contain no muscles; instead they are all hidden inside the thorax. Understanding how insects efficiently meet the high-energy demands of flight, using their remarkably complex flight motor therefore presents an exciting challenge that is of interest to both biologists and engineers.In muscles there is typically a trade-off between force production and speed, which presents a problem for insect flight. Some insect orders they have evolved power muscles that do not require neuronal activation for each contraction. These power muscles can operate at high frequencies (up to 1000 Hz in some mosquitoes), while still producing high forces as the majority of the muscle can consist of contractile apparatus. However, a consequence is that these power muscles are unable to produce rapid changes in their force production, necessary for manoeuvring flight. Instead, a myriad of small steering muscles are responsible for producing rapid changes in wing motion. Nonetheless, these steering muscles must also operate at high frequencies, while simultaneously dealing with the high power output produced by the much larger power muscles.The aim of this grant is to use an integrated approach to gain the most detailed understanding of the mechanics, function and energetics of insect flight muscle to date. We will determine how the movements, neural stiumulation, force production and efficiency of different flight muscles changes according to their role in the flight. We will compare muscles across dipteran (flies) species and other insect orders to further understand how natural selection has shaped the flight motor in species with different aerial behaviour and ecologies.Measuring all of the above parameters simultaneously in insects is currently impossible, largely due to size limitations. Instead we will use a combination of methods to measure each separately and then combine the information to give a detailed picture of muscle function. We use time-resolved microtomography, a recently developed technique that makes it possible, for the first time, to visualise and measure the movements of the internal structures inside a live, flying insect and electrophysiology to record in vivo muscle action potential. We also record wing movements allowing us to collate data across experiments by matching wingbeat parameters.These data will then be applied to in vitro work loop studies of the same muscles so that their length changes and neuronal activation can be simulated as if they were in vivo. This will allow us to determine how the muscles make use of mechanisms such as negative work in the steering muscles and elastic storage in the power muscles to increase efficiency and performance. We will also determine how the muscle's energy consumption contributes to the overall energetic cost of flight and flight manoeuvres, by measuring the rates of oxygen consumption and carbon dioxide production during tethered flight in a wind tunnel.Using an integrated approach such as this we will provide a unique insight into the functional mechanisms underlying the control and energetics of insect flight. This research will be of interest to biologists interested in how natural selection alters the function of muscles adapted for different purposes. The outputs will also provide engineers inspiration for the design of flapping unmanned air systems that are typically limited by inefficient motors.