Moth tails divert bat attack: Evolution of acoustic deflection
Edited by May R. Berenbaum, University of Illinois at Urbana-Champaign, Urbana, IL, and approved January 28, 2015 (received for review November 15, 2014)
Significance
Bats and moths have been engaged in acoustic warfare for more than 60 million y. Yet almost half of moth species lack bat-detecting ears and still face intense bat predation. We hypothesized that the long tails of one group of seemingly defenseless moths, saturniids, are an anti-bat strategy designed to divert bat attacks. Using high-speed infrared videography, we show that the spinning hindwing tails of luna moths lure echolocating bat attacks to these nonessential appendages in over half of bat–moth interactions. Further we show that long hindwing tails have independently evolved multiple times in saturniid moths. This finding expands our knowledge of antipredator deflection strategies, the limitations of bat sonar, and the extent of a long-standing evolutionary arms race.
Abstract
Adaptations to divert the attacks of visually guided predators have evolved repeatedly in animals. Using high-speed infrared videography, we show that luna moths (Actias luna) generate an acoustic diversion with spinning hindwing tails to deflect echolocating bat attacks away from their body and toward these nonessential appendages. We pit luna moths against big brown bats (Eptesicus fuscus) and demonstrate a survival advantage of ∼47% for moths with tails versus those that had their tails removed. The benefit of hindwing tails is equivalent to the advantage conferred to moths by bat-detecting ears. Moth tails lured bat attacks to these wing regions during 55% of interactions between bats and intact luna moths. We analyzed flight kinematics of moths with and without hindwing tails and suggest that tails have a minimal role in flight performance. Using a robust phylogeny, we find that long spatulate tails have independently evolved four times in saturniid moths, further supporting the selective advantage of this anti-bat strategy. Diversionary tactics are perhaps more common than appreciated in predator–prey interactions. Our finding suggests that focusing on the sensory ecologies of key predators will reveal such countermeasures in prey.
Data Availability
Data deposition: The data reported in this paper have been deposited in the Dryad Data Repository, datadryad.org (accession no. 0vn84).
Acknowledgments
We thank K. Miner, Z. Mroz, M. Eschenbrenner, and A. Acree for assistance with bat care and data analysis; G. Dewsbury, S. Epstein, D. Gluckman, D. Plotkin, and M. Standridge for assistance with moth rearing; J. McClung, E. Ortiz-Acevedo, P. Padrón, and P. Skelley for assistance with figures; R. Nuxoll and O. Bigelow for instrumentation support; E. Anderson for donating specimens; and W. Conner, M.-A. de Graaff, E. Hayden, P. Houlihan, D. Mennitt, K. Mitter, and D. Plotkin for comments and discussion. We acknowledge funding from National Science Foundation Grants IOS-1121807 (to J.R.B.) and IOS-1121739 (to A.Y.K.), postdoc support from the Florida Museum of Natural History (to J.W.B.), and undergraduate research support from the McNair Scholars Program (to A.L.K).
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Information & Authors
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Published in
Cover image: Pictured is a confocal cross-section through the intestine of a zebrafish at 120 hours postfertilization. Red, green, and gray colors indicate staining with gavaged biotin, phalloidin, and DAPI, respectively. Lindsay Marjoram et al. found that loss of function of the epigenetic regulator uhrf1 in zebrafish led to increased expression of the tnfa gene in intestinal epithelial cells. The increase led to cell shedding and apoptosis consistent with chronic inflammation. Knockdown of the tnfa gene restored epithelial cell morphology and intestinal barrier function, suggesting that loss of epigenetic regulation of tnfa might lead to chronic intestinal inflammation disorders such as inflammatory bowel disease. See the article by Marjoram et al. on pages 2770–2775. Image courtesy of Lindsay Marjoram.
Classifications
Data Availability
Data deposition: The data reported in this paper have been deposited in the Dryad Data Repository, datadryad.org (accession no. 0vn84).
Submission history
Published online: February 17, 2015
Published in issue: March 3, 2015
Keywords
Acknowledgments
We thank K. Miner, Z. Mroz, M. Eschenbrenner, and A. Acree for assistance with bat care and data analysis; G. Dewsbury, S. Epstein, D. Gluckman, D. Plotkin, and M. Standridge for assistance with moth rearing; J. McClung, E. Ortiz-Acevedo, P. Padrón, and P. Skelley for assistance with figures; R. Nuxoll and O. Bigelow for instrumentation support; E. Anderson for donating specimens; and W. Conner, M.-A. de Graaff, E. Hayden, P. Houlihan, D. Mennitt, K. Mitter, and D. Plotkin for comments and discussion. We acknowledge funding from National Science Foundation Grants IOS-1121807 (to J.R.B.) and IOS-1121739 (to A.Y.K.), postdoc support from the Florida Museum of Natural History (to J.W.B.), and undergraduate research support from the McNair Scholars Program (to A.L.K).
Notes
This article is a PNAS Direct Submission.
Authors
Competing Interests
The authors declare no conflict of interest.
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