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Jumping in planthopper and froghopper insects is propelled by a catapult-like mechanism requiring mechanical storage of energy and its quick release to accelerate the hind legs rapidly. To understand the functional biomechanics involved in these challenging movements, the internal skeleton, tendons and muscles involved were reconstructed in 3-D from confocal scans in unprecedented detail. Energy to power jumping was generated by slow contractions of hind leg depressor muscles and then stored by bending specialised elements of the thoracic skeleton that are composites of the rubbery protein resilin sandwiched between layers of harder cuticle with air-filled tunnels reducing mass. The images showed that the lever arm of the power-producing muscle changed in magnitude during jumping, but at all joint angles would cause depression, suggesting a mechanism by which the stored energy is released. This methodological approach illuminates how miniaturized components interact and function in complex and rapid movements of small animals.

Drosophila melanogaster males perform a series of courtship behaviors that, when successful, result in copulation with a female. For over a century, mutations in the yellow gene, named for its effects on pigmentation, have been known to reduce male mating success. Prior work has suggested that yellow influences mating behavior through effects on wing extension, song, and/or courtship vigor. Here, we rule out these explanations, as well as effects on the nervous system more generally, and find instead that the effects of yellow on male mating success are mediated by its effects on pigmentation of male-specific leg structures called sex combs. Loss of yellow expression in these modified bristles reduces their melanization, which changes their structure and causes difficulty grasping females prior to copulation. These data illustrate why the mechanical properties of anatomy, not just neural circuitry, must be considered to fully understand the development and evolution of behavior. More than 100 years ago, Nobel-prize winning geneticist Thomas Hunt Morgan and his colleagues discovered that some fruit flies inherited genetic mutations that caused their body color to change. The yellow flies had a mutation in one specific gene and these mutants did not only look different from normal flies, they behaved differently too. Specifically, yellow males were far less successful at mating than normal males, demonstrating for the first time that some behaviors had a genetic basis. Since then it has remained a mystery how the genetic mutations that cause yellow coloration in fruit flies lead to unsuccessful mating attempts. Geneticists have long suggested that mutations in insect pigment genes cause changes in the fly’s brain because these pigments are made from dopamine, a chemical messenger that acts in the brain. They proposed that yellow flies must have altered levels of dopamine in their brains which was causing them to fail at mating. To solve this mystery, Massey et al. used a series of genetic experiments and high speed-videos to assess how mutations in male yellow fruit flies affected their mating behavior. The experiments showed that yellow fruit flies mated poorly not because of changes in their brain but because of changes in specialized structures on their legs called sex combs. The yellow males lack melanin pigments in their sex combs, which changes their structure. As a result, the yellow males would court female flies but were then unable to grab and mount them. This explains why yellow flies often fail to mate and why fruit flies have sex combs in the first place. The study reveals the importance of scientists considering that genes that affect behavior may do so by changing anatomy rather than by altering the brain. The results also may benefit those working to control insect pests. For example, they could help insect pest managers to develop strategies that prevent reproduction in other insects that spread disease or destroy crops.

We describe the anatomy of all the primary motor neurons in the fly proboscis and characterize their contributions to its diverse reaching movements. Pairing this behavior with the wealth of Drosophila’s genetic tools offers the possibility to study motor control at single-neuron resolution, and soon throughout entire circuits. As an entry to these circuits, we provide detailed anatomy of proboscis motor neurons, muscles, and joints. We create a collection of fly strains to individually manipulate every proboscis muscle through control of its motor neurons, the first such collection for an appendage. We generate a model of the action of each proboscis joint, and find that only a small number of motor neurons are needed to produce proboscis reaching. Comprehensive control of each motor element in this numerically simple system paves the way for future study of both reflexive and flexible movements of this appendage.

The amphipod crustacean Parhyale hawaiensis is a blossoming model system for studies of developmental mechanisms and more recently regeneration. We have sequenced the genome allowing annotation of all key signaling pathways, transcription factors, and non-coding RNAs that will enhance ongoing functional studies. Parhyale is a member of the Malacostraca clade, which includes crustacean food crop species. We analysed the immunity related genes of Parhyale as an important comparative system for these species, where immunity related aquaculture problems have increased as farming has intensified. We also find that Parhyale and other species within Multicrustacea contain the enzyme sets necessary to perform lignocellulose digestion ('wood eating'), suggesting this ability may predate the diversification of this lineage. Our data provide an essential resource for further development of Parhyale as an experimental model. The first malacostracan genome will underpin ongoing comparative work in food crop species and research investigating lignocellulose as an energy source. The marine crustacean known as Parhyale hawaiensis is related to prawns, shrimps and crabs and is found at tropical coastlines around the world. This species has recently attracted scientific interest as a possible new model to study how animal embryos develop before birth and, because Parhyale can rapidly regrow lost limbs, how tissues and organs regenerate. Indeed, Parhyale has many characteristics that make it a good model organism, being small, fast-growing and easy to keep and care for in the laboratory. Several research tools have already been developed to make it easier to study Parhyale. This includes the creation of a system for using the popular gene editing technology, CRISPR, in this animal. However, one critical resource that is available for most model organisms was missing; the complete sequence of all the genetic information of this crustacean, also known as its genome, was not available. Kao, Lai, Stamataki et al. have now compiled the Parhyale genome – which is slightly larger than the human genome – and studied its genetics. Analysis revealed that Parhyale has genes that allow it to fully digest plant material. This is unusual because most animals that do this rely upon the help of bacteria. Kao, Lai, Stamataki et al. also identified genes that provide some of the first insights into the immune system of crustaceans, which protects these creatures from diseases. Kao, Lai, Stamataki et al. have provided a resource and findings that could help to establish Parhyale as a popular model organism for studying several ideas in biology, including organ regeneration and embryonic development. Understanding how Parhyale digests plant matter, for example, could progress the biofuel industry towards efficient production of greener energy. Insights from its immune system could also be adapted to make farmed shrimp and prawns more resistant to infections, boosting seafood production.

Animals acquire predictive values of sensory stimuli through reinforcement. In the brain of Drosophila melanogaster, activation of two types of dopamine neurons in the PAM and PPL1 clusters has been shown to induce aversive odor memory. Here, we identified the third cell type and characterized aversive memories induced by these dopamine neurons. These three dopamine pathways all project to the mushroom body but terminate in the spatially segregated subdomains. To understand the functional difference of these dopamine pathways in electric shock reinforcement, we blocked each one of them during memory acquisition. We found that all three pathways partially contribute to electric shock memory. Notably, the memories mediated by these neurons differed in temporal stability. Furthermore, combinatorial activation of two of these pathways revealed significant interaction of individual memory components rather than their simple summation. These results cast light on a cellular mechanism by which a noxious event induces different dopamine signals to a single brain structure to synthesize an aversive memory.

Many animals possess mechanosensory neurons that fire when a limb nears the limit of its physical range, but the function of these proprioceptive limit detectors remains poorly understood. Here, we investigate a class of proprioceptors on the Drosophila leg called hair plates. Using calcium imaging in behaving flies, we find that a hair plate on the fly coxa (CxHP8) detects the limits of anterior leg movement. By reconstructing CxHP8 axons in an electron microscopy dataset, we found that they are wired to excite posterior leg movement and inhibit anterior leg movement. Consistent with this connectivity, optogenetic activation of CxHP8 neurons elicited posterior postural reflexes, while silencing altered the swing-to-stance transition during walking. Finally, we use comprehensive reconstruction of peripheral morphology and downstream connectivity to predict the function of other hair plates distributed across the fly leg. Our results suggest that each hair plate is specialized to control specific sensorimotor reflexes that are matched to the joint limit it detects. They also illustrate the feasibility of predicting sensorimotor reflexes from a connectome with identified proprioceptive inputs and motor outputs. The physiology and behavioral function of proprioceptors that detect joint limits are not fully understood. In this study, the authors used calcium imaging, optogenetics, behavioral genetics, and the connectome to demonstrate that hair plate proprioceptors on the fly leg detect joint limits and engage circuits to drive the leg away from those limits.

The mushroom body (MB) is the center for associative learning in insects. In Drosophila , intersectional split-GAL4 drivers and electron microscopy (EM) connectomes have laid the foundation for precise interrogation of the MB neural circuits. However, investigation of many cell types upstream and downstream of the MB has been hindered due to lack of specific driver lines. Here we describe a new collection of over 800 split-GAL4 and split-LexA drivers that cover approximately 300 cell types, including sugar sensory neurons, putative nociceptive ascending neurons, olfactory and thermo-/hygro-sensory projection neurons, interneurons connected with the MB-extrinsic neurons, and various other cell types. We characterized activation phenotypes for a subset of these lines and identified a sugar sensory neuron line most suitable for reward substitution. Leveraging the thousands of confocal microscopy images associated with the collection, we analyzed neuronal morphological stereotypy and discovered that one set of mushroom body output neurons, MBON08/MBON09, exhibits striking individuality and asymmetry across animals. In conjunction with the EM connectome maps, the driver lines reported here offer a powerful resource for functional dissection of neural circuits for associative learning in adult Drosophila .

Aversive long-term memory is formed after multiple conditioning sessions spaced by a rest interval. The authors identify specific dopaminergic neurons that display oscillatory calcium activity and are required during the rest interval to allow the formation of long-term memory in the mushroom body, the olfactory memory center. A fundamental duty of any efficient memory system is to prevent long-lasting storage of poorly relevant information. However, little is known about dedicated mechanisms that appropriately trigger production of long-term memory (LTM). We examined the role of Drosophila dopaminergic neurons in the control of LTM formation and found that they act as a switch between two exclusive consolidation pathways leading to LTM or anesthesia-resistant memory (ARM). Blockade, after aversive olfactory conditioning, of three pairs of dopaminergic neurons projecting on mushroom bodies, the olfactory memory center, enhanced ARM, whereas their overactivation conversely impaired ARM. Notably, blockade of these neurons during the intertrial intervals of a spaced training precluded LTM formation. Two pairs of these dopaminergic neurons displayed sustained calcium oscillations in naive flies. Oscillations were weakened by ARM-inducing massed training and were enhanced during LTM formation. Our results indicate that oscillations of two pairs of dopaminergic neurons control ARM levels and gate LTM.

Insulin-like growth factor-binding proteins (IGFBPs) control bioavailability, activity, and distribution of insulin-like growth factor (IGF)1 and -2 through high-affinity IGFBP/IGF complexes. IGFbinding sites are found on N- and C-terminal fragments of IGFBPs, the two conserved domains of IGFBPs. The relative contributions of these domains to IGFBP/IGF complexation has been difficult to analyze, in part, because of the lack of appropriate three-dimensional structures. To analyze the effects of N- and C-terminal domain interactions, we determined several x-ray structures: first, of a ternary complex of N- and C-terminal domain fragments of IGFBP4 and IGF1 and second, of a \"hybrid\" ternary complex using the C-terminal domain fragment of IGFBP1 instead of IGFBP4. We also solved the binary complex of the N-terminal domains of IGFBP4 and IGF1, again to analyze C- and N-terminal domain interactions by comparison with the ternary complexes. The structures reveal the mechanisms of IGF signaling regulation via IGFBP binding. This finding supports research into the design of IGFBP variants as therapeutic IGF inhibitors for diseases of IGF disregulation. In IGFBP4, residues 1-38 form a rigid disulphide bond ladder-like structure, and the first five N-terminal residues bind to IGF and partially mask IGF residues responsible for the type 1 IGF receptor binding. A high-affinity IGF1-binding site is located in a globular structure between residues 39 and 82. Although the C-terminal domains do not form stable binary complexes with either IGF1 or the N-terminal domain of IGFBP4, in the ternary complex, the C-terminal domain contacts both and contributes to blocking of the IGF1 receptor-binding region of IGF1.

Insects constitute the most species-rich radiation of metazoa, a success that is due to the evolution of active flight. Unlike pterosaurs, birds and bats, the wings of insects did not evolve from legs 1 , but are novel structures that are attached to the body via a biomechanically complex hinge that transforms tiny, high-frequency oscillations of specialized power muscles into the sweeping back-and-forth motion of the wings 2 . The hinge consists of a system of tiny, hardened structures called sclerites that are interconnected to one another via flexible joints and regulated by the activity of specialized control muscles. Here we imaged the activity of these muscles in a fly using a genetically encoded calcium indicator, while simultaneously tracking the three-dimensional motion of the wings with high-speed cameras. Using machine learning, we created a convolutional neural network 3 that accurately predicts wing motion from the activity of the steering muscles, and an encoder–decoder 4 that predicts the role of the individual sclerites on wing motion. By replaying patterns of wing motion on a dynamically scaled robotic fly, we quantified the effects of steering muscle activity on aerodynamic forces. A physics-based simulation incorporating our hinge model generates flight manoeuvres that are remarkably similar to those of free-flying flies. This integrative, multi-disciplinary approach reveals the mechanical control logic of the insect wing hinge, arguably among the most sophisticated and evolutionarily important skeletal structures in the natural world. Measurements of fly muscle activity using a genetically encoded calcium indicator and high-speed imaging of wing movement were used to construct a model of the insect wing hinge and the role of steering muscles in flight control.