Convergent Evolution of Wingbeat-Powered Anti-Bat Ultrasound in the Microlepidoptera

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Abstract

Certain moth taxa can produce ultrasound to defend themselves against echolocating bats; most do so actively in response to detecting an approaching bat. Species of the deaf microlepidopteran genus Yponomeuta were recently shown to constantly produce wingbeat-powered anti-bat sounds during flight using novel wing-embedded aeroelastic tymbals (ATs). These sounds closely match acoustic warning signals of other moths, meaning Yponomeuta gain protection whilst negating the need for bat detection. Such an elegant evolutionary solution to anti-bat defence for deaf moths is unlikely to be exclusive to the Yponomeuta and their relatives. Indeed, we predicted it would be found in other microlepidoptera, a group often overlooked in terms of their defences against bats. Here we show ATs have likely evolved convergently 15 times in the microlepidoptera, including thrice in the subfamily Tineinae (Tineidae). We also present the first acoustic recordings and characterisation of four of these microlepidopteran taxa, and the first molecular phylogeny of the Tineidae. Until now the microlepidoptera have been understudied in terms of the bat-moth evolutionary arms race, but our approach of phylogenetic, morphological, and acoustic analysis indicates that many of these moths possess advanced acoustic defences. The high levels of convergence we find in AT evolution are indicative of these moths suffering strong predation pressure from bats. In fact, link the extraordinary three examples of convergence in the Tineinae to their unusual life histories and feeding ecology; these moths can spend their entire lives in bat roosts feeding, as larvae, on guano, placing them under constant predation pressure. Here we provide the first evidence that anti-bat defences are widespread in the microlepidoptera, we anticipate that this will provide a catalyst to further research on the group’s ecological relationships with bats. The bat-moth evolutionary arms race is a burgeoning field of sensory, behavioural, and evolutionary biology, with adaptations on both sides having huge scope for technological advances such as biomimetics. Through this project we open a new chapter in the field, the anti-bat adaptions of microlepidoptera.
Original languageEnglish
Article number648223
JournalFrontiers in Ecology and Evolution
Volume9
DOIs
Publication statusPublished - 3 May 2021

Bibliographical note

Funding Information:
For allowing us to examine their Lepidopteran collections, we would like to thank Bristol Museum and Art Gallery and the Natural History Museum, London, and their trustees. We offer particular thanks to Ray Barnett, Rhian Rowson, and David Lees. Funding. LO was supported during this project by the University of Bristol Graduate Teaching Assistant Ph.D. Scholarship awarded to MH and is currently supported by the Swiss National Science Foundation Spark grant CRSK-2_190855. BH was supported by a New Phytologist Trust Ph.D. studentship. MH was supported by the Biotechnology and Biological Sciences Research Council (grant BB/N009991/1) and the Engineering and Physical Sciences Research Council (grant EP/T002654/1).

Funding Information:
LO was supported during this project by the University of Bristol Graduate Teaching Assistant Ph.D. Scholarship awarded to MH and is currently supported by the Swiss National Science Foundation Spark grant CRSK-2_190855. BH was supported by

Publisher Copyright:
© Copyright © 2021 O’Reilly, Harris, Agassiz and Holderied.

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