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Elaborate traits evolve via intense selective pressure, overpowering ecological constraints. Hindwing tails that thwart bat attack have repeatedly originated in moon moths (Saturniidae), with longer tails having greater anti-predator effect. Here, we take a macroevolutionary approach to evaluate the evolutionary balance between predation pressure and possible limiting environmental factors on tail elongation. To trace the evolution of tail length across time and space, we inferred a time-calibrated phylogeny of the entirely tailed moth group (Actias + Argema) and performed ancestral state reconstruction and biogeographical analyses. We generated metrics of predation via estimates of bat abundance from nearly 200 custom-built species distribution models and environmental metrics via estimates of bioclimatic variables associated with individual moth observations. To access community science data, we developed a novel method for measuring wing lengths from un-scaled photos. Integrating these data into phylogenetically informed mixed models, we find a positive association between bat predation pressure and moth tail length and body size, and a negative association between environmental factors and these morphological traits. Regions with more insectivorous bats and more consistent temperatures tend to host longer-tailed moths. Our study provides insight into tradeoffs between biotic selective pressures and abiotic constraints that shape elaborate traits across the tree of life. 

Echolocating bats and their eared insect prey are in an acoustic evolutionary war. Moths produce anti-bat sounds that startle bat predators, signal noxiousness, mimic unpalatable models and jam bat sonar. Tiger beetles (Cicindelidae) also purportedly produce ultrasound in response to bat attacks. Here we tested 19 tiger beetle species from seven genera and showed that they produce anti-bat signals to playback of authentic bat echolocation. The dominant frequency of beetle sounds substantially overlaps the sonar calls of sympatric bats. As tiger beetles are known to produce defensive chemicals such as benzaldehyde and hydrogen cyanide, we hypothesized that tiger beetle sounds are acoustically advertising their unpalatability. We presented captive big brown bats (Eptesicus fuscus) with seven different tiger beetle species and found that 90 out of 94 beetles were completely consumed, indicating that these tiger beetle species are not aposematically signalling. Instead, we show that the primary temporal and spectral characteristics of beetle warning sounds overlap with sympatric unpalatable tiger moth (Arctinae) sounds and that tiger beetles are probably Batesian mimics of noxious moth models. We predict that many insect taxa produce anti-bat sounds and that the acoustic mimicry rings of the night sky are hyperdiverse. 

Abstract The most emblematic animal traits are often attributed to sexual selection. While this pressure is an important force, elaborated traits that have been driven solely by natural selection are less enumerated. Here, we test an elaborate trait in moths—hindwing tails—that has been studied in an anti-predator context, but that remains unstudied for its role in mating. We gave female Actias luna (Saturniidae) moths a choice between two males of differing hindwing tail treatments. In our primary experiment, males with intact tails garnered more matings than males with tails removed. This difference appears to result from damage incurred by tail removal, however, as demonstrated with additional experiments. We created a tail/no-tail experimental set where we removed tails from both males, then reglued tails to one and applied glue only to the hindwings of the other. We found no significant difference in mating success between these males. To ensure that this result was not due to the glue itself, we offered females two intact males, with glue added to the wings of one. This set also had equal mating success. We therefore do not find evidence that tails play a role in sexual selection. These results, in combination with previous research on bat-moth battles using A. luna, indicate that the non-sexually dimorphic hindwing tail was likely driven by natural selection. We suggest that future research testing multiple selective forces is needed to reveal the prevalence of natural versus sexual selection as the primary force driving trait elaboration in diverse animal taxa. 

Predators and prey exist in persistent conflict that often hinges on deception—the transmission of misleading or manipulative signals—as a means for survival. Deceptive traits are widespread across taxa and sensory systems, representing an evolutionarily successful and common strategy. Moreover, the highly conserved nature of the major sensory systems often extends these traits past single species predator–prey interactions toward a broader set of perceivers. As such, deceptive traits can provide a unique window into the capabilities, constraints and commonalities across divergent and phylogenetically-related perceivers. Researchers have studied deceptive traits for centuries, but a unified framework for categorizing different types of post-detection deception in predator–prey conflict still holds potential to inform future research. We suggest that deceptive traits can be distinguished by their effect on object formation processes. Perceptual objects are composed of physical attributes (what) and spatial (where) information. Deceptive traits that operate after object formation can therefore influence the perception and processing of either or both of these axes. We build upon previous work using a perceiver perspective approach to delineate deceptive traits by whether they closely match the sensory information of another object or create a discrepancy between perception and reality by exploiting the sensory shortcuts and perceptual biases of their perceiver. We then further divide this second category, sensory illusions, into traits that distort object characteristics along either the what or where axes, and those that create the perception of whole novel objects, integrating the what/where axes. Using predator–prey examples, we detail each step in this framework and propose future avenues for research. We suggest that this framework will help organize the many forms of deceptive traits and help generate predictions about selective forces that have driven animal form and behavior across evolutionary time. 

Traits are often caught in a dynamic tension of countervailing evolutionary pressures. Trade-offs can be imposed by predators evolutionarily curtailing the conspicuousness of a sexually selected trait, or acting in opposition to another natural selection pressure, for instance, a different predator with a divergent hunting strategy. Some moon moths (Saturniidae) have long hindwing tails that thwart echolocating bat attacks at night, allowing the moth to escape. These long tails may come at a cost, however, if they make the moth's roosting form more conspicuous to visually foraging predators during the day. To test this potential trade-off, we offered wild-caught Carolina wrens ( Thryothorus ludovicianus ) pastry dough models with real Actias luna wings that were either intact or had tails experimentally removed. We video recorded wrens foraging on models and found that moth models with tails did not experience increased detection and attack by birds. Thus, this elaborate trait, while obvious to human observers, does not seem to come at a cost of increased avian predator attention. The evolution of long hindwing tails, likely driven by echolocating predators at night, does not seem to be limited by opposing diurnal constraints. This study demonstrates the importance of testing presumed trade-offs and provides hypotheses for future testing. 

Warning signals are well known in the visual system, but rare in other modalities. Some moths produce ultrasonic sounds to warn bats of noxious taste or to mimic unpalatable models. Here, we report results from a long-term study across the globe, assaying moth response to playback of bat echolocation. We tested 252 genera, spanning most families of large-bodied moths, and document anti-bat ultrasound production in 52 genera, with eight subfamily origins described. Based on acoustic analysis of ultrasonic emissions and palatability experiments with bats, it seems that acoustic warning and mimicry are the raison d'être for sound production in most moths. However, some moths use high-duty-cycle ultrasound capable of jamming bat sonar. In fact, we find preliminary evidence of independent origins of sonar jamming in at least six subfamilies. Palatability data indicate that jamming and warning are not mutually exclusive strategies. To explore the possible organization of anti-bat warning sounds into acoustic mimicry rings, we intensively studied a community of moths in Ecuador and, using machine-learning approaches, found five distinct acoustic clusters. While these data represent an early understanding of acoustic aposematism and mimicry across this megadiverse insect order, it is likely that ultrasonically signaling moths comprise one of the largest mimicry complexes on earth. 

Abstract One of the key objectives in biological research is understanding how evolutionary processes have produced Earth’s diversity. A critical step toward revealing these processes is an investigation of evolutionary tradeoffs—that is, the opposing pressures of multiple selective forces. For millennia, nocturnal moths have had to balance successful flight, as they search for mates or host plants, with evading bat predators. However, the potential for evolutionary trade-offs between wing shape and body size are poorly understood. In this study, we used phylogenomics and geometric morphometrics to examine the evolution of wing shape in the wild silkmoth subfamily Arsenurinae (Saturniidae) and evaluate potential evolutionary relationships between body size and wing shape. The phylogeny was inferred based on 782 loci from target capture data of 42 arsenurine species representing all 10 recognized genera. After detecting in our data one of the most vexing problems in phylogenetic inference—a region of a tree that possesses short branches and no “support” for relationships (i.e., a polytomy), we looked for hidden phylogenomic signal (i.e., inspecting differing phylogenetic inferences, alternative support values, quartets, and phylogenetic networks) to better illuminate the most probable generic relationships within the subfamily. We found there are putative evolutionary trade-offs between wing shape, body size, and the interaction of fore- and hindwing (HW) shape. Namely, body size tends to decrease with increasing HW length but increases as forewing (FW) shape becomes more complex. Additionally, the type of HW (i.e., tail or no tail) a lineage possesses has a significant effect on the complexity of FW shape. We outline possible selective forces driving the complex HW shapes that make Arsenurinae, and silkmoths as a whole, so charismatic. [Anchored hybrid enrichment; Arsenurinae; geometric morphometrics; Lepidoptera; phylogenomics; Saturniidae.] 

Predators frequently must detect and localize their prey in challenging environments. Noisy environments have been prevalent across the evolutionary history of predator–prey relationships, but now with increasing anthropogenic activities noise is becoming a more prominent feature of many landscapes. Here, we use the gleaning pallid bat, Antrozous pallidus , to investigate the mechanism by which noise disrupts hunting behaviour. Noise can primarily function to mask —obscure by spectrally overlapping a cue of interest, or distract —occupy an animal's attentional or other cognitive resources. Using band-limited white noise treatments that either overlapped the frequencies of a prey cue or did not overlap this cue, we find evidence that distraction is a primary driver of reduced hunting efficacy in an acoustically mediated predator. Under exposure to both noise types successful prey localization declined by half, search time nearly tripled, and bats used 25% more sonar pulses than when hunting in ambient conditions. Overall, the pallid bat does not seem capable of compensating for environmental noise. These findings have implications for mitigation strategies, specifically the importance of reducing sources of noise on the landscape rather than attempting to reduce the bandwidth of anthropogenic noise. 

Experimental bat-moth battles reveal that sonar sensing is a driving force in the repeated evolution of silk moth hindwings. 

Abstract The acoustic environment can serve as a niche axis, structuring animal behaviour by providing or obscuring salient information. Meadow katydid choruses occupy the ultrasonic, less studied, realm of this acoustic milieu, form dense populations in some habitats and present a potential sensory challenge to co‐occurring ultrasonic‐hearing animals. Aerial‐hawking insectivorous bats foraging immediately over vegetation must listen for echoes of their prey and other cues amidst the chorus din.We experimentally created the cacophony of a katydid chorus in a katydid‐free rice paddy using an aggregation of 100 ultrasonic speakers in a 25 × 25 m grid to test the hypothesis that aerially hawking bats are averse to this noise source. We alternated between chorus‐on and chorus‐off hourly, and acoustically monitored bat activity and arthropod prey abundance.We found that our phantom katydid chorus reduced bat activity nearest the sound source by 39.3% (95% CI: 7.8%–60.0%) for species whose call spectrum fully overlapped with the chorus, and elicited marginal reductions in activity in species with only partial spectral overlap.Our study suggests that ultrasonic insect choruses degrade foraging habitat, potentially suppressing bats’ ecosystem services as consumers of pests; and, given the global distribution of meadow katydids, may provide an underappreciated force modifying animal behaviour in other grassland habitats. A freePlain Language Summarycan be found within the Supporting Information of this article.