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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.

The masked birch caterpillar, Drepana arcuata, provides an excellent opportunity to study mechanisms mediating developmental changes in social behaviour. Larvae transition from being social to solitary during the 3.sup.rd instar, concomitant with shifts in their use of acoustic communication. In this study we characterize the transcriptome of D. arcuata to initiate sociogenomic research of this lepidopteran insect. We assembled and annotated the combined larval transcriptome of \"social\" early and \"solitary\" late instars using next generation Illumina sequencing, and used this transcriptome to conduct differential gene expression analysis of the two behavioural phenotypes. A total of 211,012,294 reads generated by RNA sequencing were assembled into 231,348 transcripts and 116,079 unigenes for the functional annotation of the transcriptome. Expression analysis revealed 3300 transcripts that were differentially expressed between early and late instars, with a large proportion associated with development and metabolic processes. We independently validated differential expression patterns of selected transcripts using RT-qPCR. The expression profiles of social and solitary larvae revealed differentially expressed transcripts coding for gene products that have been previously reported to influence social behaviour in other insects (e.g. cGMP- and cAMP- dependent kinases, and bioamine receptors). This study provides the first transcriptomic resources for a lepidopteran species belonging to the superfamily Drepanoidea, and gives insight into genetic factors mediating grouping behaviour in insects.

Objective Group-living plays a key role in the success of many insects, but the mechanisms underlying group formation and maintenance are poorly understood. Here we use the masked birch caterpillar, Drepana arcuata, to explore genetic influences on social grouping. These larvae predictably transition from living in social groups to living solitarily during the 3rd instar of development. Our previous study showed a notable shift in the D. arcuata transcriptome that correlates with the transition from grouping to solitary behavior. We noted that one differentially regulated gene, octopamine receptor gene (DaOAR), is a prominent ‘social’ gene in other insect species, prompting us to test the hypothesis that DaOAR influences grouping behavior in D. arcuata . This was done using RNA interference (RNAi) methods by feeding second instar larvae synthetic dsRNAs. Results RT–qPCR analysis confirmed a significant reduction in DaOAR transcript abundance in dsRNA-fed larvae compared to controls. Behavioral trials showed that caterpillars with reduced transcript abundance of DaOAR remained solitary throughout the observation period compared to controls. These results provide evidence that regulation of the octopamine receptor gene influences social grouping in D. arcuata , and that specifically, a decrease in octopamine receptor expression triggers the larval transition from social to solitary.

Animal communication signals can be highly elaborate, and researchers have long sought explanations for their evolutionary origins. For example, how did signals such as the tail-fan display of a peacock, a firefly flash or a wolf howl evolve? Animal communication theory holds that many signals evolved from non-signalling behaviours through the process of ritualization. Empirical evidence for ritualization is limited, as it is necessary to examine living relatives with varying degrees of signal evolution within a phylogenetic framework. We examine the origins of vibratory territorial signals in caterpillars using comparative and molecular phylogenetic methods. We show that a highly ritualized vibratory signal—anal scraping—originated from a locomotory behaviour—walking. Furthermore, comparative behavioural analysis supports the hypothesis that ritualized vibratory signals derive from physical fighting behaviours. Thus, contestants signal their opponents to avoid the cost of fighting. Our study provides experimental evidence for the origins of a complex communication signal, through the process of ritualization. Many animals communicate through gestures, some caterpillars use scraping and drumming signals to ward off unwanted neighbours. Here, Scott et al . demonstrate that \"leg-like\" structures used by some caterpillar species to communicate evolved from legs that their ancestors used to walk.

Egg-laying decisions are critical for insects, and particularly those competing for limited resources. Sensory information used by females to mediate egg-laying decisions has been reported to be primarily chemical, but the role of vibration has received little attention. We tested the hypothesis that vibrational cues produced by feeding larvae occupying a seed influences egg-laying decisions amongst female cowpea beetles. This hypothesis is supported by three lines of evidence using two strains of the cowpea beetle (Callosobruchus maculatus), an Indian strain with choosy females and aggressively competing larvae and a Brazilian strain with less choosy females and larvae exhibiting an \"accommodating\" type of competition. First, in free-choice bioassays of seed selection, choosy Indian females selected control seeds (free of eggs, larvae, or egg-laying marker) over seeds with live larvae (free of eggs and egg-laying marker), but did not discriminate between control seeds and those with dead larvae. In contrast, less choosy Brazilian females showed no preference for seeds containing live or dead larvae over controls. Second, laser-doppler vibrometer recordings confirmed that larvae feeding inside seeds generate vibrations that are available to the female during egg-laying decisions. Third, during dichotomous choice experiments where artificial vibrations approximating those produced by feeding larvae were played back during seed selection, Indian females preferred immobile control seeds over vibrating seeds, but Brazilian females showed no preference. These results support the hypothesis that females use larval vibrations in their egg-laying decisions; whether these vibrations are passive cues exploited by the female, or active signals that 'steer' the behaviour of the female is unknown. We propose that vibration cues and signals could be important for host selection in insects, particularly those laying on substrates where visual or chemical cues may be unreliable. This seems to be the case with females of the cowpea beetle since visual cues are not important and chemical egg-marking does not last more than two weeks, allowing vibration cues to improve discrimination of egg-laying substrate particularly by choosy females.

Many Nymphalidae butterflies possess ears, but little is known about their hearing. The tympanal membrane of butterflies typically comprises distinct inner and outer regions innervated by auditory nerve branches NII and NIII and their respective sensory organs. Using the Blue Morpho butterfly (Morpho peleides) as a model, we characterized threshold and suprathreshold responses of NII and NIII. Both are broadly tuned to 1–20 kHz with best frequencies at 1–3 kHz, but NIII is significantly more sensitive than NII. The compound action potentials (CAPs) of both branches increase their first peak amplitudes and areas in response to higher sound levels. NII and NIII differed in their suprathreshold CAP responses to sound frequencies, with stronger responses to 1–3 and 4–6 kHz, for NIII and NII respectively; results that are consistent with tympanal membrane mechanics. These results indicate that butterflies are capable of amplitude and frequency discrimination. Both auditory branches responded to playbacks of the flight and calls of predatory birds. We propose that the ears of butterflies, like those of many vertebrate prey such as some rabbits and lizards, function primarily in predator risk assessment.

Leaf-borne vibrations are predicted to be significant for caterpillar communication and risk assessment, but the caterpillar’s vibratory landscape remains largely unknown. To address this, we used the fall armyworm Spodoptera frugiperda , as a model in our study with two main goals: (1) to characterize the vibratory landscape on a leaf in the presence of abiotic (wind and rain) and biotic (conspecifics and invertebrate predator) stimuli; and (2) to assess whether different larval instars detect and respond to those vibrations. Our findings show that abiotic and biotic vibrations were distinct from background noise, except for those produced by 1st instar larvae. Wind-induced leaf movement produced vibrations with a low-frequency and high-amplitude (< 100 Hz and 2.97 mm s −1 ), in contrast with raindrops (> 174 Hz; 3.25 mm s −1 ). The 2nd to 5th instar larvae and predatory stinkbugs moving on leaves produced vibrations with dominant frequencies ranging from 140 to 326 Hz and amplitudes from 1.42 to 2.95 mm s −1 . Furthermore, the spatial distribution of vibrations across bean leaves revealed that abiotic vibrations were more widely spread across leaves, unlike the more concentrated biotic vibrations. Regarding the caterpillar response to vibratory stimuli, caterpillars exposed to abiotic stimuli behaved differently from undisturbed caterpillars, regardless of instar. By contrast, caterpillars exposed to biotic stimuli do not respond consistently. Our findings contribute insights into a caterpillar’s vibroscape and support the hypothesis that armyworms can perceive and respond to both abiotic and biotic vibrations, filling a knowledge gap about this economically important pest species' sensory ecology.

Caterpillars of the poplar lutestring moth, Tethea or, construct leaf shelters that they defend against intruding conspecifics using a combination of vibratory signals and physical aggression. Staged interactions between a resident caterpillar and introduced conspecific were recorded with a video camera and laser vibrometer. Residents crawl towards the intruder and perform three behaviours: lateral hitting, pushing, and mandible scraping. Vibrations caused by mandible scraping result from the caterpillar repeatedly scraping opened mandibles laterally against the leaf surface in bouts lasting 1.16 ± 0.39 s, with an average of 4 ± 1 scrapes per bout. We propose that these scrapes function in leaf shelter defense against conspecifics for the following reasons: Mandible scrapes are produced only by residents; they are generated when a resident is approached by an intruder; the rate of scraping increases as the intruder approaches the shelter; and residents in all trials retain their shelters, with the intruder leaving the leaf within 127.9 ± 104.3 s from the beginning of the trial. The function and evolutionary origins of vibration-mediated territoriality in caterpillars are discussed. [PUBLICATION ABSTRACT]

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.

The masked birch caterpillar, Drepana arcuata (Lepidoptera: Drepanidae) is an excellent model for studying vibratory communication and sociality in larval insects. Vibratory communication occurs throughout development, but the functions of signals are reported to change as larvae change from gregarious to solitary lifestyles. To better understand the sensory ecology of these caterpillars, it is important to study their life history. Here, we describe the morphological and behavioral characteristics of larvae by confirming the number of instars, identifying their distinguishing morphological features, and noting changes in feeding and shelter construction. Five instars were confirmed based on the number of head capsules collected for individuals throughout development, and by using Dyar’s rule, which predicts the number of instars based on geometric growth patterns of head capsules. Frequency distributions of head capsule widths showed five separate peaks, indicating that this is a useful parameter for distinguishing between instars. Other morphological features including body length, shape, and banding patterns of head capsules, and morphology of thoracic verrucae are helpful in distinguishing among instars. Feeding behavior changes from leaf skeletonization in first and second instars to leaf cutting in fourth and fifth instars, with third instars transitioning between these feeding styles as they grow. Early instars typically construct communal silken shelters whereas late instars live solitarily in leaf shelters. These results provide essential life history information on the masked birch caterpillar that will enable future investigations on the proximate and ultimate mechanisms associated with social behavior and communication in larval insects.