Butterflies and moths (Lepidoptera) are one of the major superradiations of insects, comprising nearly 160,000 described extant species. As herbivores, pollinators, and prey, Lepidoptera play a fundamental role in almost every terrestrial ecosystem. Lepidoptera are also indicators of environmental change and serve as models for research on mimicry and genetics. They have been central to the development of coevolutionary hypotheses, such as butterflies with flowering plants and moths’ evolutionary arms race with echolocating bats. However, these hypotheses have not been rigorously tested, because a robust lepidopteran phylogeny and timing of evolutionary novelties are lacking. To address these issues, we inferred a comprehensive phylogeny of Lepidoptera, using the largest dataset assembled for the order (2,098 orthologous protein-coding genes from transcriptomes of 186 species, representing nearly all superfamilies), and dated it with carefully evaluated synapomorphy-based fossils. The oldest members of the Lepidoptera crown group appeared in the Late Carboniferous (∼300 Ma) and fed on nonvascular land plants. Lepidoptera evolved the tube-like proboscis in the Middle Triassic (∼241 Ma), which allowed them to acquire nectar from flowering plants. This morphological innovation, along with other traits, likely promoted the extraordinary diversification of superfamily-level lepidopteran crown groups. The ancestor of butterflies was likely nocturnal, and our results indicate that butterflies became day-flying in the Late Cretaceous (∼98 Ma). Moth hearing organs arose multiple times before the evolutionary arms race between moths and bats, perhaps initially detecting a wide range of sound frequencies before being co-opted to specifically detect bat sonar. Our study provides an essential framework for future comparative studies on butterfly and moth evolution.
Insects are capable of detecting a broad range of acoustic signals transmitted through air, water, or solids. Auditory sensory organs are morphologically diverse with respect to their body location, accessory structures, and number of sensilla, but remarkably uniform in that most are innervated by chordotonal organs. Chordotonal organs are structurally complex Type I mechanoreceptors that are distributed throughout the insect body and function to detect a wide range of mechanical stimuli, from gross motor movements to air-borne sounds. At present, little is known about how chordotonal organs in general function to convert mechanical stimuli to nerve impulses, and our limited understanding of this process represents one of the major challenges to the study of insect auditory systems today. This report reviews the literature on chordotonal organs innervating insect ears, with the broad intention of uncovering some common structural specializations of peripheral auditory systems, and identifying new avenues for research. A general overview of chordotonal organ ultrastructure is presented, followed by a summary of the current theories on mechanical coupling and transduction in monodynal, mononematic, Type 1 scolopidia, which characteristically innervate insect ears. Auditory organs of different insect taxa are reviewed, focusing primarily on tympanal organs, and with some consideration to Johnston's and subgenual organs. It is widely accepted that insect hearing organs evolved from pre-existing proprioceptive chordotonal organs. In addition to certain non-neural adaptations for hearing, such as tracheal expansion and cuticular thinning, the chordotonal organs themselves may have intrinsic specializations for sound reception and transduction, and these are discussed. In the future, an integrated approach, using traditional anatomical and physiological techniques in combination with new methodologies in immunohistochemistry, genetics, and biophysics, will assist in refining hypotheses on how chordotonal organs function, and, ultimately, lead to new insights into the peripheral mechanisms underlying hearing in insects.
We provide evidence for conspecific acoustic communication in caterpillars. Larvae of the common hook-tip moth, Drepana arcuata (Drepanoidea), defend silk nest sites from conspecifics by using ritualized acoustic displays. Sounds are produced by drumming the mandibles and scraping the mandibles and specialized anal ''oars'' against the leaf surface. Staged interactions between a resident and intruder resulted in escalated acoustic ''duels'' that were typically resolved within minutes, but sometimes extended for several hours. Resident caterpillars generally won territorial disputes, regardless of whether they had built the nest, but relatively large intruders occasionally displaced residents from their nests. All evidence is consistent with acoustic signaling serving a territorial function. As with many vertebrates, ritualized signaling appears to allow contestants to resolve contests without physical harm. Comparative evidence indicates that larval acoustic signaling may be widespread throughout the Lepidoptera, meriting consideration as a principal mode of communication for this important group of insects.
Caterpillars have long been used as models for studying animal defence. Their impressive armour, including flamboyant warning colours, poisonous spines, irritating sprays, and mimicry of plant parts, snakes and bird droppings, has been extensively documented. But research has mainly focused on visual and chemical displays. Here we show that some caterpillars also exhibit sonic displays. During simulated attacks, 45% of 38 genera and 33% of 61 species of silk and hawkmoth caterpillars (Bombycoidea) produced sounds. Sonic caterpillars are found in many distantly-related groups of Bombycoidea, and have evolved four distinct sound types- clicks, chirps, whistles and vocalizations. We propose that different sounds convey different messages, with some designed to warn of a chemical defence and others, to startle predators. This research underscores the importance of exploring acoustic communication in juvenile insects, and provides a model system to explore how different signals have evolved to frighten, warn or even trick predators.
Acoustic signaling is widespread in bark beetles (Scolytinae), although little is known about the physical characteristics of signals, how they are transmitted, and how they differ among behavioural contexts. Signals were studied in the male mountain pine beetle (Dendroctonus ponderosae Hopkins, 1902) during stress, male–female, and male–male interactions. Sounds are broadband with significant energy in the ultrasound (peaks between 15 and 26 kHz) and low amplitude (55 and 47 dB SPL at 2 and 4 cm, respectively), indicating that signaling functions at close range. Signal trains vary among contexts primarily in the proportions of chirp types. Chirps were categorized as being simple or interrupted, with the former having significantly lower tooth strike rates and shorter chirp durations. Stress chirps are predominantly simple with characteristics resembling other insect disturbance signals. Male–female interactions begin with the male producing predominantly interrupted chirps prior to gallery entrance, followed by simple chirps. Male–male (rivalry) chirps are predominantly simple, with evidence of antiphonal calling. Substrate-borne vibrations were detectable with a laser-doppler vibrometer at short distances (1–3 cm), suggesting that sensory organs could be tuned to either air or substrate-borne vibrations. These results have important implications for future research on the function and reception of acoustic signals in bark beetles.
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