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Nature has evolved efficient strategies to synthesize complex mineralized structures that exhibit exceptional damage tolerance. One such example is found in the hypermineralized hammer-like dactyl clubs of the stomatopods, a group of highly aggressive marine crustaceans. The dactyl clubs from one species, Odontodactylus scyllarus, exhibit an impressive set of characteristics adapted for surviving high-velocity impacts on the heavily mineralized prey on which they feed. Consisting of a multiphase composite of oriented crystalline hydroxyapatite and amorphous calcium phosphate and carbonate, in conjunction with a highly expanded helicoidal organization of the fibrillar chitinous organic matrix, these structures display several effective lines of defense against catastrophic failure during repetitive high-energy loading events.

Key Points Hepatocyte growth factor (HGF) and its tyrosine kinase receptor MET (also known as HGF receptor) mediate invasive growth, a complex programme in which cells lose contacts with their neighbours, mobilize towards adjacent surroundings, resist apoptotic insults and proliferate. During development, HGF and MET are essential for the growth and survival of epithelial cell types and for the migration of muscle progenitors. In adult physiology, MET exerts a trophic activity that attenuates tissue damage and promotes the regeneration of several organs. In tumours, MET stimulates the motility and survival of cancer cells as well as angiogenesis, thereby acting as a powerful expedient for neoplastic invasion and production of secondary metastases. MET gain-of-function genetic lesions can also be selected to maintain the transformed phenotype of some primary tumours, which seem to be 'addicted' to continued MET activity for their relentless growth. MET signals are channelled by an unconventional multifunctional docking site consisting of two tyrosines that, when phosphorylated, recruit a wide spectrum of transducers. Interaction with the GRB2-associated-binding protein 1 (GAB1) multi-adaptor protein is critical for transduction of most MET signalling pathways, whereas tissue-specific interactions with other surface partners such as the α6β4 integrin and the CD44 adhesion molecule regulate quantitative modulation of downstream signalling and cytoskeletal compartmentalization, respectively. MET signals emanate not only from the plasma membrane but also from endosomal compartments, and MET internalization seems to be required for efficient activation and proper subcellular localization of distal transducers such as extracellular signal-regulated kinases (ERKs) and signal transducer and activator of transcription 3 (STAT3). MET also undergoes other trafficking events — including extracellular shedding, intracellular cleavage, ubiquitylation, degradation and membrane recycling — which regulate the strength of MET activation and the ensuing robustness of MET-dependent signals. In distinct cells and tissues, specific activities that are controlled by MET seem to be fulfilled by dedicated signalling cascades, with some transducers dominating over others according to context, timing and biological complexity. This suggests that the specificity of MET-dependent responses is determined, at least in part, by qualitative differences in signalling outputs. The MET receptor promotes tissue remodelling by integrating growth, survival and migration cues in response to environmental stimuli or cell-autonomous perturbations. The versatility of MET-mediated biological responses is sustained by qualitative and quantitative signal modulation, which can be exploited in regenerative medicine and cancer therapy. The MET tyrosine kinase receptor (also known as the HGF receptor) promotes tissue remodelling, which underlies developmental morphogenesis, wound repair, organ homeostasis and cancer metastasis, by integrating growth, survival and migration cues in response to environmental stimuli or cell-autonomous perturbations. The versatility of MET-mediated biological responses is sustained by qualitative and quantitative signal modulation. Qualitative mechanisms include the engagement of dedicated signal transducers and the subcellular compartmentalization of MET signalling pathways, whereas quantitative regulation involves MET partnering with adaptor amplifiers or being degraded through the shedding of its extracellular domain or through intracellular ubiquitylation. Controlled activation of MET signalling can be exploited in regenerative medicine, whereas MET inhibition might slow down tumour progression.

Quantitative biomechanical models can identify control parameters that are used during movements, and movement parameters that are encoded by premotor neurons. We fit a mathematical dynamical systems model including subsyringeal pressure, syringeal biomechanics and upper-vocal-tract filtering to the songs of zebra finches. This reduces the dimensionality of singing dynamics, described as trajectories (motor ‘gestures’) in a space of syringeal pressure and tension. Here we assess model performance by characterizing the auditory response ‘replay’ of song premotor HVC neurons to the presentation of song variants in sleeping birds, and by examining HVC activity in singing birds. HVC projection neurons were excited and interneurons were suppressed within a few milliseconds of the extreme time points of the gesture trajectories. Thus, the HVC precisely encodes vocal motor output through activity at the times of extreme points of movement trajectories. We propose that the sequential activity of HVC neurons is used as a ‘forward’ model, representing the sequence of gestures in song to make predictions on expected behaviour and evaluate feedback. The auditory response of song premotor HVC neurons in sleeping birds, and HVC activity in singing birds, is synchronized with particular moments of vocal motor movements as defined by a dynamical systems model of song production; this HVC activity could be used as a ‘forward’ model to predict behaviour and evaluate feedback. What gives birds the urge to sing The complex songs produced by birds such as zebra finches require precisely timed vocal control. One theory for how such timing is achieved is that neurons in the HVC, the brain region essential for the learning and production of bird song, produce a 'clock' signal to pace movements. Daniel Margoliash and colleagues present evidence in support of an alternate model: using a combination of biophysical modelling of the avian syrinx and recordings in asleep and awake birds, they find that HVC activity is precisely synchronized with singing. This suggests that rather than encoding time, these neurons implement a predictive, 'forward' sensorimotor model of song.

The pars tuberalis of the pituitary gland is the regulatory hub for seasonal reproduction in birds and mammals. Although fish also exhibit robust seasonal responses, they do not possess an anatomically distinct pars tuberalis. Here we report that the saccus vasculosus of fish is a seasonal sensor. We observe expression of key genes regulating seasonal reproduction and rhodopsin family genes in the saccus vasculosus of masu salmon. Immunohistochemical studies demonstrate that all of these genes are expressed in the coronet cells of the saccus vasculosus, suggesting the existence of a photoperiodic signalling pathway from light input to neuroendocrine output. In addition, isolated saccus vasculosus has the capacity to respond to photoperiodic signals, and its removal abolishes photoperiodic response of the gonad. Although the physiological role of the saccus vasculosus has been a mystery for several centuries, our findings indicate that the saccus vasculosus acts as a sensor of seasonal changes in day length in fish. The saccus vasculosus is a circumventricular organ of the hypothalamus of many jawed fish whose function has remained a mystery for more than 300 years. Here the authors provide evidence that the saccus vasculosus functions as a sensor of seasonal changes in day length.

Ticks are second only to mosquitoes as vectors of disease to humans and animals. Tick host detection is mainly ascribed to Haller's organ, a complex sensory structure on the tick foreleg that detects odors, carbon dioxide and heat, but these host detection mechanisms are not well understood. There is anecdotal evidence that ticks and other ectoparasites are attracted to heat, but it has never been demonstrated that they use radiant heat to detect hosts at a distance. In fact, previous attempts to do this have concluded that radiant heat was not used by ticks. Here we use a novel thermotaxis assay to investigate the detection range, temperature dependence and repellent sensitivity of heat perception in ticks and to identify the sensory organ responsible for this sense. We show that Amblyomma americanum and Dermacentor variabilis ticks can locate a human from several meters away by radiant heat sensed by the part of Haller's organ known as the capsule, a covered spherical pit organ. An aperture in the capsule cover confers directionality and highly reflective interior surfaces of the capsule concentrate radiation on the sensilla to sharpen directionality and increase sensitivity. Commercial insect repellents provide an effective means of personal protection against potentially infectious tick bites by hindering host-seeking behavior. Low concentrations of the insect repellents DEET, picaridin, 2-undecanone, citronellal and nootkatone eliminate thermotaxis without affecting olfaction-stimulated host-seeking behavior. Our results demonstrate that the tick Haller's organ capsule is a radiant heat sensor used in host-finding and that repellents disrupt this sense at concentrations that do not disrupt olfaction. We anticipate that this discovery will significantly aid insect repellent research and provide novel targets for the development of innovative integrated pest management programs and personal protection strategies for ectoparasites and vector-borne disease.

Adult moths from framily Spingidae (i.e. hawkmoths or sphinx moths) commonly feed on flower nectar through an extended proboscis, often several centimeters in length and longer than the body of the moth. Feeding on a viscous liquid (nectar) through a long and narrow tube is a challenging fluid dynamic problem and the subject of long-running scientific investigation. Here we characterized the relationship between proboscis submergence depth and nectar drinking rate in Manduca sexta hawkmoths. Video recordings of moth feeding bouts were collected and neural networks were used to extract data by object localization, tracking the location of the nectar meniscus and moths’ proboscis tips. We found that although feeding rates vary among bouts, the variation was not associated with proboscis submergence depth. These results show that despite the theoretical possibility of fluid uptake through the walls of the proboscis, such effects do not have a substantial effect on nectar uptake rate, and suggest that nectar must traverse the full length of the proboscis.

Chengjiangocaris kunmingensis sp. nov. and Fuxianhuia xiaoshibaensis sp. nov.— early Cambrian fuxianhuiid fossils from a new Lagerstätte in Yunnan, China—show that ancestral arthropods had cephalic organization that included an antenniform first appendage, which corresponds to the deutocerebral head segment of modern arthropods. Early arthropods with a modern look The evolution of the structure of the head in arthropods — jointed-limbed creatures such as insects and crustaceans — has been a matter of debate for some while. One point of contention is whether the spectacular 'great appendages' that adorn the front of the heads of some Cambrian forms correspond to the appendages of modern arthropods. The fuxianhuiids, primitive fossil arthropods from the Cambrian of China, are emerging as a pivotal group in the study of the early arthropod anatomy. A series of remarkable new discoveries is continuing that trend. In these fuxianhuiids, the carapace is stripped away to reveal the underlying body structure. The creatures were organized very much along the lines of modern arthropods, with no 'great appendages'. This suggests that the exaggerated appendages may have been distinct features of even more primitive arthropods than the fuxianhuiids, that were then lost. The organization of the head provides critical data for resolving the phylogenetic relationships and evolutionary history of extinct and extant euarthropods 1 , 2 . The early Cambrian-period fuxianhuiids are regarded as basal representatives of stem-group Euarthropoda 3 , 4 , 5 , 6 , 7 , and their anterior morphology therefore offers key insights for reconstructing the ancestral condition of the euarthropod head 1 , 2 , 3 , 8 , 9 , 10 , 11 . However, the paired post-antennal structures in Fuxianhuia protensa remain controversial 3 , 8 , 10 ; they have been interpreted as both ‘great appendages’ 1 , 2 and as gut diverticulae 4 , 12 , 13 . Here we describe Chengjiangocaris kunmingensis sp. nov. and Fuxianhuia xiaoshibaensis sp. nov. from a new early Cambrian (Stage 3) fossil Lagerstätte in Yunnan, China. Numerous specimens of both species show a unique ‘taphonomic dissection’ of the anterodorsal head shield, revealing the cephalic organization in detail. We demonstrate the presence of a pair of specialized post-antennal appendages (SPAs) in the fuxianhuiid head, which attach at either side of the posteriorly directed mouth, behind the hypostome. Preserved functional articulations indicate a well-defined but restricted range of limb movement, suggestive of a simple type of sweep feeding. The organization of the SPAs in fuxianhuiids is incompatible with the (deutocerebral) anterior raptorial appendages of megacheirans 2 , 9 , 14 , 15 , and argue against the presence of protocerebral limbs in the fuxianhuiids 1 , 2 , 9 . The positions of the fuxianhuiid antennae and SPAs indicate that they are segmentally homologous to the deutocerebral and tritocerebral appendages of crown-group Euarthropoda respectively 2 , 11 , 16 , 17 . These findings indicate that antenniform deutocerebral appendages with many podomeres are a plesiomorphic feature of the ancestral euarthropod head.

The structure of the stomatopod dactyl club—an ultrafast, hammer-like device used by the animal to shatter hard seashells—offers inspiration for impact-tolerant ceramics. Here, we present the micromechanical principles and related micromechanisms of deformation that impart the club with high impact tolerance. By using depth-sensing nanoindentation with spherical and sharp contact tips in combination with post-indentation residual stress mapping by Raman microspectroscopy, we show that the impact surface region of the dactyl club exhibits a quasi-plastic contact response associated with the interfacial sliding and rotation of fluorapatite nanorods, endowing the club with localized yielding. We also show that the subsurface layers exhibit strain hardening by microchannel densification, which provides additional dissipation of impact energy. Our findings suggest that the club’s macroscopic size is below the critical size above which Hertzian brittle cracks are nucleated. Nanoindentation and spectroscopy measurements show that the impact surface of the dactyl club—a hammer-like device that stomatopods use to shatter hard seashells—has a quasi-plastic response that enhances the damage tolerance of the clubs.

North American porcupines are well known for their specialized hairs, or quills that feature microscopic backward-facing deployable barbs that are used in self-defense. Herein we show that the natural quill’s geometry enables easy penetration and high tissue adhesion where the barbs specifically contribute to adhesion and unexpectedly, dramatically reduce the force required to penetrate tissue. Reduced penetration force is achieved by topography that appears to create stress concentrations along regions of the quill where the cross sectional diameter grows rapidly, facilitating cutting of the tissue. Barbs located near the first geometrical transition zone exhibit the most substantial impact on minimizing the force required for penetration. Barbs at the tip of the quill independently exhibit the greatest impact on tissue adhesion force and the cooperation between barbs in the 0–2 mm and 2–4 mm regions appears critical to enhance tissue adhesion force. The dual functions of barbs were reproduced with replica molded synthetic polyurethane quills. These findings should serve as the basis for the development of bio-inspired devices such as tissue adhesives or needles, trocars, and vascular tunnelers where minimizing the penetration force is important to prevent collateral damage.

The butterfly genus Hypolimnas features iridescent blue colouration in some areas of its dorsal wings. Here, we analyse the mechanisms responsible for such colouration on the dorsal wings of Hypolimnas salmacis and experimentally demonstrate that the lower thin lamina in the white cover scales causes the blue iridescence. This outcome contradicts other studies reporting that the radiant blue in Hypolimnas butterflies is caused by complex ridge-lamellar architectures in the upper lamina of the cover scales. Our comprehensive optical study supported by numerical calculation however shows that scale stacking primarily induces the observed colour appearance of Hypolimnas salmacis .