Abstract
Bats and moths provide a textbook example of predator-prey evolutionary arms races, demonstrating adaptations, and counter adaptations on both sides. The evolutionary responses of moths to the biosonar-led hunting strategies of insectivorous bats include convergently evolved hearing structures tuned to detect bat echolocation frequencies. These allow many moths to detect hunting bats and manoeuvre to safety, or in the case of some taxa, respond by emitting sounds which startle bats, jam their biosonar, and/or warn them of distastefulness. Until now, research has focused on the larger macrolepidoptera, but the recent discovery of wingbeat-powered anti-bat sounds in a genus of deaf microlepidoptera (Yponomeuta), suggests that the speciose but understudied microlepidoptera possess further and more widespread anti-bat defences. Here we demonstrate that wingbeat-powered ultrasound production, likely providing an anti-bat function, appears to indeed be spread widely in the microlepidoptera; showing that acoustically active structures (aeroelastic tymbals, ATs) have evolved in at least three, and likely four different regions of the wing. Two of these tymbals are found in multiple microlepidopteran superfamilies, and remarkably, three were found in a single subfamily. We document and characterise sound production from four microlepidopteran taxa previously considered silent. Our findings demonstrate that the microlepidoptera contribute their own unwritten chapters to the textbook bat-moth coevolutionary arms race.
Highlights
Roeder’s seminal discovery of anti-bat hearing (Roeder and Treat, 1957) sparked research into the defences of nocturnal moths against echolocating bats in the bat-moth acoustic evolutionary arms race
Yponomeuta provide the first example of constitutive acoustic aposematism in the batmoth arms race (O’Reilly et al, 2019). This elegant defence solution for unpalatable, deaf microlepidoptera is unlikely to be exclusive to the Yponomeutidae and here we investigate whether other microlepidopteran taxa possess yet undocumented defences based on aeroelastic tymbals (ATs)
We identified ATs in four different locations on microlepidopteran wings (Figure 2) and named them as follows: (1) Forewing Subcostal Tymbal (FST) at the forewing base between the subcostal and radial veins in the cell directly above the discal cell; (2) Forewing Discal Tymbal (FDT) directly within the apex of the discal cell itself; (3) Forewing Cubital Tymbal (FCT) in the cell directly below the first cubital veins; and (4) Hindwing Cubital Tymbal (HCT) at the base of the hindwing in the cell directly below first cubital veins
Summary
Roeder’s seminal discovery of anti-bat hearing (Roeder and Treat, 1957) sparked research into the defences of nocturnal moths against echolocating bats in the bat-moth acoustic evolutionary arms race. A recent surge of new discoveries has arisen in this arms race: taxa other than the Arctiinae have been shown to produce anti-bat sounds (Barber and Kawahara, 2013; Corcoran and Hristov, 2014; O’Reilly et al, 2019), the hindwing “tails” of some moths have been discovered to act as acoustic decoys (Barber et al, 2015; Lee and Moss, 2016), and the acoustic absorptive power of moth scales as acoustic metamaterials has emerged as a fascinating and complex new area of research (Zeng et al, 2011; Ntelezos et al, 2017; Shen et al, 2018; Neil et al, 2020a,b). Microlepidoptera are under significant predation pressure from bats
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