Tempo and mode of antibat ultrasound production and sonar jamming in the diverse hawkmoth radiation

Kawahara, Akito Y.; Barber, Jesse R.

doi:10.1073/pnas.1416679112

Cited by 64 publications

(100 citation statements)

References 63 publications

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“…However, >65,000 species of nocturnal moths lack this acoustic defense (22) yet still face intense bat predation (23). Our data suggest that diversionary anti-bat defenses can be as successful as other acoustic strategies in this arms race (24)(25)(26). Additional taxa with hindwing tails, including Lepidoptera and lacewings (27), might also be diverting predator attack to nonessential appendages.…”

Section: Resultsmentioning

confidence: 91%

Moth tails divert bat attack: Evolution of acoustic deflection

Barber

Leavell

Keener

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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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.antipredator defense | bat-moth interactions | Lepidoptera | Saturniidae P redators are under pressure to perform incapacitating initial strikes to thwart prey escape. It is thought that prey, in turn, have evolved conspicuous colors or markings to deflect predator attack to less vulnerable body regions (1, 2). Eyespots are a wellknown class of proposed deflection marks (3), which are found in a variety of taxa, including Lepidoptera (3) and fishes (4), but only recently have experiments convincingly demonstrated that these color patterns redirect predatory assault. Eyespots on artificial butterfly (5) and fish (4) prey draw strikes of avian and fish predators. Eyespots on the wing margins of woodland brown butterflies (Lopinga achine) lure the attacks of blue tits (Cyanistes caeruleus) (6). Brightly colored lizard tails also divert avian predator attacks to this expendable body region (7).Deflection coloration is unlikely to be an effective strategy against echolocating bats, as these predators have scotopic vision and poor visual acuity unsuited for prey localization and discrimination (8). Most bats rely on echoes from their sonar cries to image prey and other objects in their environment-they live in an auditory world (9). Thus, we would expect a deflection strategy, effective against bats, to present diversionary acoustic signatures to these hearing specialists. Weeks (10) proposed that saturniid hindwing tails might serve to divert bat attacks from essential body parts. We hypothesized that saturniid tails, spinning behind a flying moth (Movie S1) and reflecting sonar calls, serve as either a highly contrasting component of the primary echoic target or as an alternative target. We predicted that bats would aim their attacks at moth tails, instead of the wings or body, durin...

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Section: Resultsmentioning

confidence: 91%

Moth tails divert bat attack: Evolution of acoustic deflection

Barber

Leavell

Keener

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

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“…Further, when the clicks of chemically defended C. tenera fall within this 2 ms window, they do interfere with echolocation in experienced bats (Ratcliffe and Fullard, 2005). Sound production is not limited to tiger moths, and new evidence suggests that some sphinx moths also deter bats by producing many clicks per unit time with a stridulatory organ (see Glossary; Barber and Kawahara, 2013;Kawahara and Barber, 2015).…”

Section: Sound Production In Moths: Defence Courtship and Sexual Antmentioning

confidence: 99%

Evolutionary escalation: the bat–moth arms race

Hofstede

Ratcliffe

2016

Journal of Experimental Biology

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Echolocation in bats and high-frequency hearing in their insect prey make bats and insects an ideal system for studying the sensory ecology and neuroethology of predator-prey interactions. Here, we review the evolutionary history of bats and eared insects, focusing on the insect order Lepidoptera, and consider the evidence for antipredator adaptations and predator counter-adaptations. Ears evolved in a remarkable number of body locations across insects, with the original selection pressure for ears differing between groups. Although cause and effect are difficult to determine, correlations between hearing and life history strategies in moths provide evidence for how these two variables influence each other. We consider life history variables such as size, sex, circadian and seasonal activity patterns, geographic range and the composition of sympatric bat communities. We also review hypotheses on the neural basis for antipredator behaviours (such as evasive flight and sound production) in moths. It is assumed that these prey adaptations would select for counter-adaptations in predatory bats. We suggest two levels of support for classifying bat traits as counter-adaptations: traits that allow bats to eat more eared prey than expected based on their availability in the environment provide a low level of support for counter-adaptations, whereas traits that have no other plausible explanation for their origination and maintenance than capturing defended prey constitute a high level of support. Specific predator counter-adaptations include calling at frequencies outside the sensitivity range of most eared prey, changing the pattern and frequency of echolocation calls during prey pursuit, and quiet, or 'stealth', echolocation.

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“…According to Rothschild & Jordan (), it is fully developed in the closest relatives of Hyles ( Chaerocina, Rothschild & Jordan, Euchloron Boisduval, [1875] and Xylophanes Hübner, [1819]; Kawahara et al . ; Kawahara & Barber ). In the genus Hyles , the arolium can be fully developed, reduced and apparently non‐functional or completely absent in different species, and the condition of this structure in H. salangensis could provide evidence to help resolve the phylogenetic affinities of the species.…”

Section: Introductionmentioning

confidence: 99%

Museum archives revisited: Central Asiatic hawkmoths reveal exceptionally high late Pliocene species diversification (Lepidoptera, Sphingidae)

et al. 2017

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Three high‐elevation Hyles species of Central Asia have proven difficult to sample, and thus, only a limited number of specimens are available for study. Ancient DNA techniques were applied to sequence two mitochondrial genes from ‘historic’ museum specimens of Hyles gallii, Hyles renneri and Hyles salangensis to elucidate the phylogenetic relationships of these species. This approach enabled us to include the holotypes and paratypes. The status of H. salangensis as a species endemic to a mountain range north of Kabul in Afghanistan is confirmed by this study. It is most closely related to Hyles nicaea and H. gallii, and quite distant from the clade comprising the species from Hyles vespertilio to Hyles tithymali, despite this group and H. salangensis both completely lacking an arolium on the pretarsus. Our results show that the samples assigned to H. renneri and Hyles livornica tatsienluica are conspecific and so we reinstate Hyles tatsienluica stat. nov. as the valid name for this species and synonymize H. renneri syn. nov. with it. This study shows that the distribution range postulated for H. tatsienluica extends from Nepal well into the mountains of south‐western China. The distribution ranges of H. livornica and H. tatsienluica overlap. The study confirms the previously proposed synonymies of Hyles nepalensis, Hyles gallii intermedia and Hyles gallii tibetanica with H. gallii. Extensive species sampling (over 80% of Hyles species) in this study allowed additional analyses. The dated phylogeny reveals the global Hyles hawkmoth radiation to be much more recent than previously thought: it began in the Late Miocene and culminated in a Pleistocene burst of diversification in the Northern Hemisphere. Ancestral ranges of basal nodes were reconstructed as highly equivocal, but the Neotropics has the highest probability in the two oldest nodes. Although the origins of the Madagascan and Australian species also remain ambiguous, a large crown clade of fifteen species was reconstructed to have originated in the Palaearctic. The wide distribution ranges of the two migratory species, H. livornica and H. gallii, appear to blur any traces of the biogeographic origin of the clades containing these species. Specialization in larval host plant use onto particular plant families from the ancestral condition ‘polyphagous’ may have led to an increased rate of speciation and phylogenetic diversification in three subgroups of Hyles (the Hawaiian clade, the Hyles centralasiae group and the Hyles euphorbiae complex).

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Tempo and mode of antibat ultrasound production and sonar jamming in the diverse hawkmoth radiation

Cited by 64 publications

References 63 publications

Moth tails divert bat attack: Evolution of acoustic deflection

Moth tails divert bat attack: Evolution of acoustic deflection

Evolutionary escalation: the bat–moth arms race

Museum archives revisited: Central Asiatic hawkmoths reveal exceptionally high late Pliocene species diversification (Lepidoptera, Sphingidae)

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