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

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Our aim is to use an integrated approach to produce the most detailed understanding of the mechanics, function and efficiency of insect flight muscles. Key objectives we aim to answer are: how do the tiny steering muscles control the wingbeat by efficiently managing the power produced by the much larger power muscles? To what extent do the flight muscles make use of elastic storage and how does muscle and whole organism efficiency change during manoeuvres? How do the functional mechanics and efficiency of the flight muscles change across insect species and orders?

We will measure in vivo muscle strains using synchrotron-based, time-resolved microtomography; in vivo muscle action potentials using electrophysiology; and whole organism in vivo energetics using respirometry. Across all in vivo experiments we will record and calculate 3D wing kinematics using high-speed cameras. This will allow us to determine how the measured parameters change with different wingbeats, and crucially to synchronise measurements across experiments by matching wingbeats. The in vivo muscle measurements will be used to simulate in vivo muscle oscillations using the in vitro work loop approach to calculate muscle work, elastic storage and efficiency.

We will initially use blowflies (Calliphora vicinia) due to its appropriate size for the different experimental setups and the large body of time-resovled microtomography data already collected by the PI. However, we will expand to other dipteran species and insect orders to allow a comparative approach. We will aim to understand how differences in the functional mechanics of the flight muscles across species relates to differences in their flight behaviour, such as hovering in hoverflies, something that Calliphora cannot do. We will also determine how muscle mechanics and flight efficiency changes in insect orders with low wingbeat frequencies but asynchronous or synchronous flight muscles.

Obtaining an integrative understanding of the means by which insects control their flight and attain their high manoeuvrability is of broad scientific relevance and will have impact on the aeronautic industry, the general public and on the researchers employed on the grant, in addition to the benefits to the academic community (see Academic Beneficiaries).

APPLIED LINKS WITH THE POTENTIAL TO BENEFIT INDUSTRY, IMPROVE HEALTH AND DEVELOP THE 3Rs
Our insights into the mechanisms and energetics underlying the control of the wingstroke and their relationship to flight manoeuvres will be important to engineers developing autonomous unmanned air systems (UAS) for exploration, surveillance and rescue work in situations where manned flights could be unsafe or expensive. Engineers are adopting a bio-inspired approach to the design of UAS and knowledge about how the muscular and sensory systems are efficiently integrated in insects, will guide design optimization in these devices. The UK has been at the forefront of advances in our understanding insect flight aerodynamics since the pioneering work of Weis-Fogh and Ellington (University of Cambridge) and more recent work by the Oxford Animal Flight Group. Our research will help to maintain and promote the UK as a leader in insect flight research and make the UK an attractive prospect for UAS development funding.

The knowledge gained in this project will help in the development and refinement of computational models of muscle contraction. Our work is focused on how healthy muscle tissue works, which is central to developing an understanding of malfunctions that occur during ageing and disease. In all modes of locomotion, energetics and locomotor performance are linked via an energy transduction chain. Therefore, whilst our work is on flying insects the models developed should be generally applicable to other modes of locomotion and the development of an understanding of locomotor energetics in the field. Developing accurate models of muscle contraction may allow some animal experiments to be replaced and in other cases refined or reduced as simulations may allow research efforts involving animal research to be better designed.

IMPACT ON THE GENERAL PUBLIC
Animal locomotion is a topic that consistently arouses public interest. We are committed to using our research to inspire young audiences to take an interest in science. Our work will have a positive impact by informing the general public about technological advances in science and the applications of biological research. We will engage with the public through open lectures, school visits and exhibitions at museums in Oxford and Leeds. We will also apply for the Royal Society Summer Science exhibit, which attracts over 14,000 people, including 2000 school students.

OTHER SPECIFIC IMPACTS
Specific beneficiaries include the two PDRAs who will develop their scientific careers with BBSRC funding. They will be involved in a research project that crosses discipline boundaries in biology. They will benefit from working closely with laboratories in two different leading institutions (as verified by the 2014 REF). The research will also impact on the training of undergraduates who will benefit from carrying out final year research projects within our laboratories.