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

昆虫是地球上种类最多、经济上最重要的一类动物，毫无疑问，它们取得巨大成功的原因之一是它们令人难以置信的飞行能力，在机动性和控制力方面，它们通常远远超过脊椎动物。在人类眨眼的时间里，一只苍蝇可以拍打翅膀50次，每次拍打翅膀都是用无数微小的肌肉来驱动和控制的，有些肌肉只有人类的头发那么细。与会飞的脊椎动物不同，昆虫的翅膀没有肌肉；相反，它们都隐藏在胸腔内。因此，了解昆虫如何有效地利用它们非常复杂的飞行马达来满足飞行的高能量需求，是生物学家和工程师都感兴趣的一项令人兴奋的挑战。在肌肉中，通常在力量产生和速度之间存在权衡，这对昆虫的飞行提出了一个问题。有些昆虫进化出了动力肌肉，每次收缩都不需要神经元激活。这些动力肌肉可以在高频率下工作（某些蚊子的频率高达1000赫兹），同时仍然产生很大的力量，因为大部分肌肉可以由收缩装置组成。然而，结果是这些力量肌肉不能产生快速的力量产生变化，这是操纵飞行所必需的。相反，无数的小操纵肌肉负责产生翅膀运动的快速变化。尽管如此，这些转向肌肉也必须在高频率下工作，同时处理由更大的动力肌肉产生的高功率输出。这项资助的目的是使用一种综合的方法来获得迄今为止昆虫飞行肌肉的力学、功能和能量学的最详细的理解。我们将确定不同飞行肌肉的运动、神经刺激、力量产生和效率如何根据它们在飞行中的作用而变化。我们将比较双翅目（苍蝇）物种和其他昆虫目的肌肉，以进一步了解自然选择如何在具有不同空中行为和生态的物种中塑造飞行马达。在昆虫中同时测量上述所有参数目前是不可能的，主要是由于尺寸限制。相反，我们将使用多种方法分别测量每种方法，然后将这些信息结合起来，给出肌肉功能的详细图像。我们使用时间分辨显微断层扫描技术，这是一项最近发展起来的技术，这使得它第一次可以可视化和测量活体飞行昆虫内部结构的运动，并通过电生理学记录体内肌肉动作电位。我们还记录了翅膀的运动，使我们能够通过匹配翼拍参数来整理实验中的数据。然后，这些数据将应用于相同肌肉的体外工作循环研究，以便模拟它们的长度变化和神经元激活，就像在体内一样。这将使我们能够确定肌肉如何利用转向肌的负功和动力肌的弹性储存等机制来提高效率和性能。我们还将通过测量在风洞中系绳飞行时的氧气消耗和二氧化碳产生率，来确定肌肉的能量消耗如何对飞行和飞行动作的总体能量消耗做出贡献。利用这样的综合方法，我们将为昆虫飞行控制和能量学的功能机制提供独特的见解。对自然选择如何改变适应不同目的的肌肉功能感兴趣的生物学家将对这项研究感兴趣。研究结果还将为工程师们提供设计扑翼无人飞行系统的灵感，这些系统通常受低效电机的限制。

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.