Bats and moths in the real world: neuronal responses as adaptations to predation

蝙蝠和昆虫之间的相互作用长期以来一直吸引着进化生物学家。蝙蝠使用回声定位来探测和跟踪夜间昆虫，全世界大约70%的蝙蝠物种吃昆虫。在防御方面，至少有7个目的昆虫进化出了耳朵，可以接收回声定位蝙蝠发出的超声波频率。这些耳朵通常结构简单，但非常有效地触发逃避行为，减少昆虫被吃掉的风险。耳朵在蛾类中的研究最多，其中1-4个感觉细胞向中枢神经系统发送信号，然后可以触发一系列行为反应，从逃离信号源到不可预测的复杂循环动作。蝙蝠和飞蛾之间的相互作用通常被视为进化的军备竞赛，蝙蝠回声定位呼叫的适应性驱动昆虫听觉反应的适应性，这反过来又塑造了蝙蝠回声定位信号的进一步进化。到目前为止，大多数关于蝙蝠和飞蛾之间相互作用的研究都是在实验室中进行的。我们的目标是研究这些相互作用的性质，这是很重要的，因为蝙蝠回声定位呼叫在现场和实验室条件下有很大的不同。因此，我们将使用飞蛾作为生物麦克风，记录蝙蝠飞行路线沿着听觉神经元的反应。我们将测试蛾检测蝙蝠物种的回声定位呼叫（具有不同的频率，时间和强度参数）的距离是否取决于信号设计。我们可以精确地量化检测距离，因为我们可以通过测量麦克风阵列的到达时间差来精确地在三维空间中确定蝙蝠的位置。我们还可以通过使用测量麦克风来计算蝙蝠在已知位置的叫声强度，从而测量触发飞蛾神经反应的声压级。我们还将通过使用两个摄像机和红外线照明记录蛾的飞行路径来量化蛾在黑暗中使用的规避策略。然后，我们可以对飞蛾使用的逃跑策略进行分类，并将其与蝙蝠使用的信号设计联系起来。这些方法将使我们能够测试这样一个假设，即飞蛾会从远处的蝙蝠身上飞走，只有当蝙蝠靠近时才会进行不可预测的逃跑动作（因此会发出更强烈的信号）。我们的第一个视频记录了一只飞蛾躲避蝙蝠的攻击，显示它使用了一种先前描述的方法来避免飞机在混战中的攻击！我们将把我们的知识从现场带到实验室，在更可控的条件下测试我们的预测。我们将回放蝙蝠对飞蛾的攻击过程。我们最近发表在《当代生物学》上的研究表明，飞蛾可以根据声源的强度改变它们的听觉反应。在低声强下，蛾耳膜对低频敏感，在较高的声强下，它们对较高的频率更敏感。听觉灵敏度的这种变化完全出乎意料。从适应性的角度来看，这些变化是完全有意义的，然而，蝙蝠在寻找昆虫时使用的频率往往比寻找昆虫时更高。我们的现场录音将给出一个准确的图片如何信号设计的变化在猎物捕获，并通过监测鼓膜的反应（通过激光测振仪），我们可以确定是否同时响应操作在神经水平上通过记录从听觉神经。我们认为，理解捕食者-猎物的相互作用可以通过在自然条件下进行研究来最好地推进。我们的工作将确定蛾听觉如何响应蝙蝠回声定位领域，如何蛾响应行为蝙蝠调用已知的结构和强度，以及蛾是否可以调整自己的听觉反应，以最好地检测蝙蝠在积极的方式。

Interactions between bats and insects have long fascinated evolutionary biologists. Bats use echolocation to detect and track nocturnal insects, and about 70% of bat species worldwide eat insects. In defence, insects in at least 7 orders have evolved ears that pick up the ultrasonic frequencies emitted by echolocating bats. These ears are often simple in structure, but highly effective for triggering escape behaviours that reduce the risk of the insect being eaten. Ears have been most studied in moths, where 1-4 sensory cells send signals to the central nervous system, which can then trigger a range of behavioural responses ranging from flight away from the signal source to unpredictable complex looping manoeuvres. Interactions between bats and moths are often viewed as an evolutionary arms race, with adaptations in the echolocation calls of bats driving adaptations in the hearing responses of insects, which in turn shape the further evolution of echolocation signals in bats. To date, most work on interactions between bats and moths has taken place in the laboratory. We aim to study these interactions in nature, and this is important because bat echolocation calls differ substantially in field and laboratory conditions. We will therefore use moths as biological microphones, recording responses of auditory neurones along the flight paths of bats. We will test whether the distance at which moths detect the echolocation calls of bat species (with differing frequency, time and intensity parameters) depends on signal design. We can quantify detection distances accurately because we can pinpoint the bat's position accurately in 3-dimensions by measuring time-of-arrival differences at an array of microphones. We can also calculate the intensity of the bat calls at known positions by using a measuring microphone, allowing us to measure the sound pressure level that triggers a neural response in the moth. We will also quantify the evasive manoeuvres used by moths in the dark by recording their flight paths using two video cameras and infrared lighting. We can then categorise the escape manoeuvres used by moths, and relate these to signal designs used by bats. These methods will allow us to test the hypothesis that moths fly away from distant bats, and only perform unpredictable escape manoeuvres when bats are close by (and hence emitting more intense signals). Our first video recording of a moth evading a bat attack has shown it to use a manoeuvre previously described as a method to avoid attack in dogfights by aircraft! We will take our knowledge from the field into the laboratory to test our predictions under more controlled conditions. We will play back some of the attack sequences emitted by bats to moth preparations. Our recent work, published in Current Biology, suggests that moths can change their hearing responses in relation to the intensity of the sound source. At low sound intensities, moth ear membranes are sensitive to low frequencies, at higher intensities they become more sensitive to higher frequencies. Such changes in hearing sensitivity were totally unexpected. The changes make perfect sense from an adaptive perspective however / bats often use higher frequencies when they home in on insects than when they are searching for them. Our field recordings will give an accurate picture of how signal design changes in prey capture, and by monitoring responses of the eardrum (by laser vibrometry) we can establish whether simultaneous responses operate at the neural level by recording from the auditory nerve. We believe that understanding predator-prey interactions can best advance by performing studies in natural conditions. Our work will determine how moth hearing responds to bat echolocation in the field, how moths respond behaviourally to bat calls of known structure and intensity, and whether moths can adjust their auditory responses to best detect bats in an active manner.