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225669691

10.1093/BEHECO/ARAA056

Socially foraging bats discriminate between group members based on search-phase echolocation calls

© The Author(s) 2020. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Original Article

Behavioral Ecology

210956970

10.1016/J.CUB.2019.12.038

Luminance Information Is Required for the Accurate Estimation of Contrast in Rapidly Changing Visual Contexts

Visual perception scales with changes in the visual stimulus, or contrast, irrespective of background illumination. However, visual perception is challenged when adaptation is not fast enough to deal with sudden declines in overall illumination, for example, when gaze follows a moving object from bright sunlight into a shaded area. Here, we show that the visual system of the fly employs a solution by propagating a corrective luminance-sensitive signal. We use in vivo 2-photon imaging and behavioral analyses to demonstrate that distinct OFF-pathway inputs encode contrast and luminance. Predictions of contrast-sensitive neuronal responses show that contrast information alone cannot explain behavioral responses in sudden dim light. The luminance-sensitive pathway via the L3 neuron is required for visual processing in such rapidly changing light conditions, ensuring contrast constancy when pure contrast sensitivity underestimates a stimulus. Thus, retaining a peripheral feature, luminance, in visual processing is required for robust behavioral responses.

Current Biology

218890576

10.1098/RSPB.2020.0488

Universal metabolic constraints shape the evolutionary ecology of diving in animals

Diving as a lifestyle has evolved on multiple occasions when air-breathing terrestrial animals invaded the aquatic realm, and diving performance shapes the ecology and behaviour of all air-breathing aquatic taxa, from small insects to great whales. Using the largest dataset yet assembled, we show that maximum dive duration increases predictably with body mass in both ectotherms and endotherms. Compared to endotherms, ectotherms can remain submerged for longer, but the mass scaling relationship for dive duration is much steeper in endotherms than in ectotherms. These differences in diving allometry can be fully explained by inherent differences between the two groups in their metabolic rate and how metabolism scales with body mass and temperature. Therefore, we suggest that similar constraints on oxygen storage and usage have shaped the evolutionary ecology of diving in all air-breathing animals, irrespective of their evolutionary history and metabolic mode. The steeper scaling relationship between body mass and dive duration in endotherms not only helps explain why the largest extant vertebrate divers are endothermic rather than ectothermic, but also fits well with the emerging consensus that large extinct tetrapod divers (e.g. plesiosaurs, ichthyosaurs and mosasaurs) were endothermic.

Proceedings of The Royal Society B: Biological Sciences

219331149

10.3390/MD18060298

Uncovering the Core Microbiome and Distribution of Palmerolide in Synoicum adareanum Across the Anvers Island Archipelago, Antarctica

Polar marine ecosystems hold the potential for bioactive compound biodiscovery, based on their untapped macro- and microorganism diversity. Characterization of polar benthic marine invertebrate-associated microbiomes is limited to few studies. This study was motivated by our interest in better understanding the microbiome structure and composition of the ascidian, Synoicum adareanum, in which palmerolide A (PalA), a bioactive macrolide with specificity against melanoma, was isolated. PalA bears structural resemblance to a hybrid nonribosomal peptide-polyketide that has similarities to microbially-produced macrolides. We conducted a spatial survey to assess both PalA levels and microbiome composition in S. adareanum in a region of the Antarctic Peninsula near Anvers Island (64°46′ S, 64°03′ W). PalA was ubiquitous and abundant across a collection of 21 ascidians (3 subsamples each) sampled from seven sites across the Anvers Island Archipelago. The microbiome composition (V3–V4 16S rRNA gene sequence variants) of these 63 samples revealed a core suite of 21 bacterial amplicon sequence variants (ASVs)—20 of which were distinct from regional bacterioplankton. ASV co-occurrence analysis across all 63 samples yielded subgroups of taxa that may be interacting biologically (interacting subsystems) and, although the levels of PalA detected were not found to correlate with specific sequence variants, the core members appeared to occur in a preferred optimum and tolerance range of PalA levels. These results, together with an analysis of the biosynthetic potential of related microbiome taxa, describe a conserved, high-latitude core microbiome with unique composition and substantial promise for natural product biosynthesis that likely influences the ecology of the holobiont.

Marine Drugs

215756159

10.1098/RSBL.2020.0063

Brilliant angle-independent structural colours preserved in weevil scales from the Swiss Pleistocene

Extant weevils exhibit a remarkable colour palette that ranges from muted monochromatic tones to rainbow-like iridescence, with the most vibrant colours produced by three-dimensional photonic nanostructures housed within cuticular scales. Although the optical properties of these nanostructures are well understood, their evolutionary history is not fully resolved, in part due to a poor knowledge of their fossil record. Here, we report three-dimensional photonic nanostructures preserved in brightly coloured scales of two weevils, belonging to the genus Phyllobius or Polydrusus, from the Pleistocene (16–10 ka) of Switzerland. The scales display vibrant blue, green and yellow hues that resemble those of extant Phyllobius/Polydrusus. Scanning electron microscopy and small-angle X-ray scattering analyses reveal that the subfossil scales possess a single-diamond photonic crystal nanostructure. In extant Phyllobius/Polydrusus, the near-angle-independent blue and green hues function primarily in crypsis. The preservation of far-field, angle-independent structural colours in the Swiss subfossil weevils and their likely function in substrate matching confirm the importance of investigating fossil and subfossil photonic nanostructures to understand the evolutionary origins and diversification of colours and associated behaviours (e.g. crypsis) in insects.

Biology Letters

2749079

10.1126/SCIADV.1500709

Blue reflectance in tarantulas is evolutionarily conserved despite nanostructural diversity

Natural selection on structural color in tarantulas resulted in convergence on color through diverse structural mechanisms. Slight shifts in arrangement within biological photonic nanostructures can produce large color differences, and sexual selection often leads to high color diversity in clades with structural colors. We use phylogenetic reconstruction, electron microscopy, spectrophotometry, and optical modeling to show an opposing pattern of nanostructural diversification accompanied by unusual conservation of blue color in tarantulas (Araneae: Theraphosidae). In contrast to other clades, blue coloration in phylogenetically distant tarantulas peaks within a narrow 20-nm region around 450 nm. Both quasi-ordered and multilayer nanostructures found in different tarantulas produce this blue color. Thus, even within monophyletic lineages, tarantulas have evolved strikingly similar blue coloration through divergent mechanisms. The poor color perception and lack of conspicuous display during courtship of tarantulas argue that these colors are not sexually selected. Therefore, our data contrast with sexual selection that typically produces a diverse array of colors with a single structural mechanism by showing that natural selection on structural color in tarantulas resulted in convergence on similar color through diverse structural mechanisms.

Science Advances

220520365

10.1073/PNAS.2006771117

Multiple origins of green coloration in frogs mediated by a novel biliverdin-binding serpin

Significance Green coloration of vertebrates is normally attributed to pigments and structural components inside skin chromatophores cells. However, these components do not account for the vivid blue-green colors of hundreds of species of frogs with sparse chromatophores. Our study shows that green coloration originates in proteins of the serpin superfamily that bind the pigment biliverdin, modulating its absorbance properties. Using a South American treefrog, we demonstrated that these serpins have a clear ecological role in modulating the reflectance properties and rendering animals cryptic in the foliage even in the near-infrared portion of the spectrum. These findings open up exciting research perspectives both in biochemistry and evolution of serpins, as well as in the study of extracellular protein-mediated coloration in vertebrates. Many vertebrates have distinctive blue-green bones and other tissues due to unusually high biliverdin concentrations—a phenomenon called chlorosis. Despite its prevalence, the biochemical basis, biology, and evolution of chlorosis are poorly understood. In this study, we show that the occurrence of high biliverdin in anurans (frogs and toads) has evolved multiple times during their evolutionary history, and relies on the same mechanism—the presence of a class of serpin family proteins that bind biliverdin. Using a diverse combination of techniques, we purified these serpins from several species of nonmodel treefrogs and developed a pipeline that allowed us to assemble their complete amino acid and nucleotide sequences. The described proteins, hereafter named biliverdin-binding serpins (BBS), have absorption spectra that mimic those of phytochromes and bacteriophytochromes. Our models showed that physiological concentration of BBSs fine-tune the color of the animals, providing the physiological basis for crypsis in green foliage even under near-infrared light. Additionally, we found that these BBSs are most similar to human glycoprotein alpha-1-antitrypsin, but with a remarkable functional diversification. Our results present molecular and functional evidence of recurrent evolution of chlorosis, describe a biliverdin-binding protein in vertebrates, and introduce a function for a member of the serpin superfamily, the largest and most ubiquitous group of protease inhibitors.

Proceedings of the National Academy of Sciences of the United States of America

215789794

10.1126/SCIENCE.AAY6912

The Ccr4-Not complex monitors the translating ribosome for codon optimality

Coupling translation and mRNA decay Gene expression requires messenger RNAs (mRNAs)—DNA-derived blueprints of genes—to be translated by protein-producing ribosomes. The levels of mRNAs are tightly regulated, in part by controlling their half-lives. In eukaryotic cells, mRNA half-life is largely linked to translational efficiency, but the mechanism underlying this link has remained elusive. Buschauer et al. used cryo–electron microscopy and RNA sequencing to show how a key regulator of mRNA degradation, the Ccr4-Not complex, monitors the ribosome during mRNA translation. They found that the Not5 subunit directly binds to a ribosomal site exposed specifically during inefficient decoding, thereby triggering mRNA degradation. Analysis of mutants revealed the importance of this sensing mechanism for mRNA homeostasis. Science, this issue p. eaay6912 A protein complex binds to ribosomes that lack bound tRNAs, thus connecting translation elongation problems and mRNA decay. INTRODUCTION The tightly controlled process of gene expression requires messenger RNAs (mRNAs), which represent DNA-derived blueprints for polypeptides, to be translated by the protein-producing machinery of the cell, the ribosomes. Therefore, protein levels depend largely on cellular mRNA levels, and the control of mRNA decay is one of the most critical processes for setting the overall level of gene expression. Half-lives of mRNAs vary greatly between different transcripts, and regulation of the mRNA decay rate is intimately connected to the elongation phase of mRNA translation. To that end, codon optimality has been established as a key parameter for determining mRNA half-life in multiple eukaryotic organisms. It has also been established that the timely decay of short-lived mRNAs enriched with nonoptimal codons requires the Ccr4-Not complex. Ccr4-Not is an essential protein complex, with its best understood role in mRNA degradation, where it serves as the major cytoplasmic 3′-poly(A)-tail deadenylase that initiates decay of most mRNAs. By deadenylation and subsequent activation of the mRNA decapping machinery, the Ccr4-Not complex renders mRNAs accessible to the major degrading exonucleases, such as Xrn1 on the 5′ end and the exosome on the 3′ end. The molecular mechanism underlying codon optimality monitoring and coordination with mRNA decay by the Ccr4-Not complex has remained elusive. RATIONALE Because nonoptimal codons affect decoding kinetics of the ribosome and mRNA degradation occurs largely cotranslationally, it is highly plausible that codon optimality is directly monitored on the ribosome. In addition, a direct physical link between the participating Ccr4-Not complex and the ribosome has been suggested previously, and the Not4 subunit of the complex, an E3 ligase, ubiquitinates the eS7 protein of the 40S ribosomal subunit in yeast. Therefore, we set out to gain insights into the connection between the Ccr4-Not complex and the translation machinery in the context of mRNA homeostasis by combining cryo–electron microscopy (cryo-EM), ribosome profiling, and biochemical analysis. RESULTS We used affinity-purified native Ccr4-Not–ribosome complexes from Saccharomyces cerevisiae for analysis by cryo-EM and found that recruitment of Ccr4-Not to the ribosome occurs via the Not5 subunit. The N terminus of Not5—in particular, a three α-helix bundle—interacted specifically with the ribosomal E-site, and deletion of the Not5 N-terminus resulted in the loss of stable ribosome association of the Ccr4-Not complex. However, ubiquitination of the small ribosomal subunit protein eS7 through the Not4 subunit still occurred. The Not5 interaction involved the ribosomal protein eS25 of the small subunit, in addition to transfer RNA (tRNA) and ribosomal RNAs (rRNAs). We found that Ccr4-Not interacts with both initiating and elongating ribosomes. In either case, Not5 engaged the E-site only when the ribosome adopted a distinct conformation lacking accommodated tRNA in the A-site, indicative of impaired decoding kinetics. Ribosome profiling revealed that low-optimality codons were enriched in the A-site in the Ccr4-Not–bound elongating ribosomes. This observation explained the low A-site tRNA occupancy observed with cryo-EM and suggested a link to codon optimality monitoring. Consistently, using mRNA stability assays, we found that loss of Not5 resulted in the inability of the mRNA degradation machinery to sense codon optimality. The observed dysregulation of mRNA half-life was detected upon Not5 deletion, Not5 N-terminal deletion, eS25 deletion, and loss of eS7 ubiquitination by Not4, which apparently serves as an upstream prerequisite for further Ccr4-Not activity on the ribosome. In addition, mRNA decapping was found to be impaired in these mutants, which confirmed that, in this pathway, Ccr4-Not triggers decapping downstream of optimality monitoring. CONCLUSION Our analysis elucidates a direct physical link between the mRNA decay–mediating Ccr4-Not complex and the ribosome. Dependent on preceding ubiquitination of eS7 by the Not4 subunit, the Ccr4-Not complex binds (via the Not5 subunit) specifically to the ribosomal E-site when the A-site lacks tRNA because of slow decoding kinetics. This state of the ribosome occurs in the presence of nonoptimal codons in the A-site, which explains the shorter half-lives of transcripts enriched in nonoptimal codons. Thus, our findings provide mechanistic insights into the coordination of translation efficiency with mRNA stability through the Ccr4-Not complex. Ccr4-Not couples translation efficiency to mRNA degradation. When ribosomes encounter nonoptimal codons, low decoding efficiency leads to an increased likelihood of dissociation of the E-site tRNA before the cognate tRNA is accommodated in the A-site. As a result, the ribosomal E-site adopts a specific conformation, which is recognized by the Ccr4-Not complex through the N-terminus of its Not5 subunit, eventually triggering mRNA degradation by Xrn1. Control of messenger RNA (mRNA) decay rate is intimately connected to translation elongation, but the spatial coordination of these events is poorly understood. The Ccr4-Not complex initiates mRNA decay through deadenylation and activation of decapping. We used a combination of cryo–electron microscopy, ribosome profiling, and mRNA stability assays to examine the recruitment of Ccr4-Not to the ribosome via specific interaction of the Not5 subunit with the ribosomal E-site in Saccharomyces cerevisiae. This interaction occurred when the ribosome lacked accommodated A-site transfer RNA, indicative of low codon optimality. Loss of the interaction resulted in the inability of the mRNA degradation machinery to sense codon optimality. Our findings elucidate a physical link between the Ccr4-Not complex and the ribosome and provide mechanistic insight into the coupling of decoding efficiency with mRNA stability.

Science

214686810

10.1016/J.ANBEHAV.2020.02.011

Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes

The gut microbiome is structured by social groups in a variety of host taxa. Whether this pattern is driven by relatedness, similar diets or shared social environments is under debate because few studies have had access to the data necessary to disentangle these factors in wild populations. We investigated whether diet, relatedness or the 1 m proximity network best explains differences in the gut microbiome among 45 female colobus monkeys in eight social groups residing at Boabeng-Fiema, Ghana. We combined demographic and behavioural data collected during May – August 2007 and October 2008 – April 2009 with 16S rRNA sequencing of faecal samples collected during the latter part of each observation period. Depending on the beta diversity index, social group identity explained 19–28% of the variation in gut microbiome beta diversity. When comparing the predictive power of dietary dissimilarity, relatedness and connectedness in the 1 m proximity network, the models with social connectedness received the strongest support, even in our analyses that excluded within-group dyads. This novel finding indicates that microbes may be transmitted during intergroup encounters, which could occur either indirectly via shared environments or directly via social contact. Lastly, some of the gut microbial taxa that appear to be transmitted via 1 m proximity are associated with digestion of plant material. Further research is needed to investigate whether this type of gut microbe transmission yields health benefits, which could provide an incentive for the formation and maintenance of social bonds within and between social groups.

Animal Behaviour

155103947

10.1039/C9SM00566H

Broadband omnidirectional light reflection and radiative heat dissipation in white beetles Goliathus goliatus.

Structural whiteness, stemming from biologically evolutionarily refined structures, provides inspiration for designing promising, reflectance-based materials. White beetles Goliathus goliatus, which can survive in high-temperature-equatorial forests, may suggest undiscovered new physical mechanisms for thermoregulation. Their scales' whiteness is created by the exquisite shell/hollow cylinder structure with two thermoregulatory effects, contributing to a lower equilibrium temperature of elytra under direct sunlight. In the visible regime, they enhance the broadband omnidirectional reflection significantly by synergetic structural effects originating from the thin-film interference, Mie resonance and total reflection. In the mid-infrared (MIR) regime, white scales act as antireflective layers to increase the emissivity in the MIR range, enabling the elytra to reradiate heat to the environment and help the beetles reduce their temperature by as much as ∼7.8 °C in air. These biological strategies for thermoregulation could provide new approaches for bioinspired coatings towards passive radiative cooling.

Soft Matter

225625568

10.1093/BEHECO/ARAA068

Juvenile social dynamics reflect adult reproductive strategies in bottlenose dolphins

The juvenile period is a challenging life-history stage, especially in species with a high degree of fission–fusion dynamics, such as bottlenose dolphins, where maternal protection is virtually absent. Here, we examined how juvenile male and female bottlenose dolphins navigate this vulnerable period. Specifically, we examined their grouping patterns, activity budget, network dynamics, and social associations in the absence of adults. We found that juveniles live in highly dynamic groups, with group composition changing every 10 min on average. Groups were generally segregated by sex, and segregation was driven by same-sex preference rather than opposite-sex avoidance. Juveniles formed strong associations with select individuals, especially kin and same-sex partners, and both sexes formed cliques with their preferred partners. Sex-specific strategies in the juvenile period reflected adult reproductive strategies, in which the exploration of potential social partners may be more important for males (which form long-term alliances in adulthood) than females (which preferentially associate with kin in adulthood). Females spent more time alone and were more focused on foraging than males, but still formed close same-sex associations, especially with kin. Males cast a wider social net than females, with strong same-sex associations and many male associates. Males engaged in more affiliative behavior than females. These results are consistent with the social bonds and skills hypothesis and suggest that delayed sexual maturity in species with relational social complexity may allow individuals to assess potential associates and explore a complex social landscape without the risks associated with sexual maturity (e.g., adult reproductive competition; inbreeding).

Behavioral Ecology

6717249

10.1016/J.CUB.2006.08.068

Character Displacement Promotes Cooperation in Bacterial Biofilms

Resource competition within a group of cooperators is expected to decrease selection for cooperative behavior but can also result in diversifying selection for the use of different resources, which in turn could retard the breakdown of cooperation. Diverse groups are likely to be less susceptible to invasion by noncooperating social cheats: First, competition repression resulting from character displacement may provide less of a selective advantage to cheating; second, cheats may trade off the ability to exploit cooperators that specialize in one type of resource against cooperators that specialize in another ; third, diverse communities of any kind may have higher invasion resistance because there are fewer resources available for an invader to use . Furthermore, diverse groups are likely to be more productive than clonal groups if a wider range of total resources are being used . We addressed these issues by using the cooperative trait of biofilm formation in Pseudomonas fluorescens. Character displacement through resource competition evolved within biofilms; productivity increased with increasing character displacement, and diverse biofilms were less susceptible to invasion by cheats. These results demonstrate that diversification into different ecological niches can minimize selection against cooperation in the face of local resource competition.

Current Biology

207950844

10.1242/JEB.210807

Communication versus waterproofing: the physics of insect cuticular hydrocarbons

ABSTRACT Understanding the evolution of complex traits is among the major challenges in biology. One such trait is the cuticular hydrocarbon (CHC) layer in insects. It protects against desiccation and provides communication signals, especially in social insects. CHC composition is highly diverse within and across species. To understand the adaptive value of this chemical diversity, we must understand how it affects biological functionality. So far, CHCs have received ample research attention, but their physical properties were little studied. We argue that these properties determine their biological functionality, and are vital to understanding how CHC composition affects their adaptive value. We investigated melting behaviour and viscosity of CHCs from 11 ant species using differential scanning calorimetry and a novel microrheological technique. CHCs began melting below −45°C, and often were entirely liquid only above 30°C. Thus, they formed a solid–liquid mixture under ambient conditions, which contrasts to previous assumptions of entirely solid layers in many species. This may be adaptive as only biphasic CHC layers ensure uniform coating of the insect body, which is necessary for waterproofing. CHC viscosity was mostly between 0.1 and 0.2 Pa s−1, thus similar to motor oils. Surprisingly, chemically different CHC profiles had similar viscosities, suggesting that a certain viscosity level is adaptive and ensures that communication signals can be perceived. With this study, we draw attention to the importance of studying the physics of CHC layers. Only by understanding how chemical and physical mechanisms enable CHC functionality can we understand the causes and consequences of CHC diversification. Summary: Cuticular hydrocarbons protect insects from desiccation and allow chemical communication, and contain both liquid and solid parts. This complex phase behaviour appears vital to ensure biological functioning.

The Journal of Experimental Biology

224810479

10.1038/S41598-020-74469-Z

Free-standing spider silk webs of the thomisid Saccodomus formivorus are made of composites comprising micro- and submicron fibers

Our understanding of the extraordinary mechanical and physico-chemical properties of spider silk is largely confined to the fibers produced by orb-weaving spiders, despite the diversity of foraging webs that occur across numerous spider families. Crab spiders (Thomisidae) are described as ambush predators that do not build webs, but nevertheless use silk for draglines, egg cases and assembling leaf-nests. A little-known exception is the Australian thomisid Saccodomus formivorus, which constructs a basket-like silk web of extraordinary dimensional stability and structural integrity that facilitates the capture of its ant prey. We examined the physical and chemical properties of this unusual web and revealed that the web threads comprise microfibers that are embedded within a biopolymeric matrix containing additionally longitudinally-oriented submicron fibers. We showed that the micro- and submicron fibers differ in their chemical composition and that the web threads show a remarkable lateral resilience compared with that of the major ampullate silk of a well-investigated orb weaver. Our novel analyses of these unusual web and silk characteristics highlight how investigations of non-model species can broaden our understanding of silks and the evolution of foraging webs.

Scientific Reports

215411481

10.1038/S41467-020-15522-3

The Scaly-foot Snail genome and implications for the origins of biomineralised armour

The Scaly-foot Snail, Chrysomallon squamiferum , presents a combination of biomineralised features, reminiscent of enigmatic early fossil taxa with complex shells and sclerites such as sachtids, but in a recently-diverged living species which even has iron-infused hard parts. Thus the Scaly-foot Snail is an ideal model to study the genomic mechanisms underlying the evolutionary diversification of biomineralised armour. Here, we present a high-quality whole-genome assembly and tissue-specific transcriptomic data, and show that scale and shell formation in the Scaly-foot Snail employ independent subsets of 25 highly-expressed transcription factors. Comparisons with other lophotrochozoan genomes imply that this biomineralisation toolkit is ancient, though expression patterns differ across major lineages. We suggest that the ability of lophotrochozoan lineages to generate a wide range of hard parts, exemplified by the remarkable morphological disparity in Mollusca, draws on a capacity for dynamic modification of the expression and positioning of toolkit elements across the genome. The Scaly-foot Snail, Chrysomallon squamiferum , is a model for understanding the evolution of biomineralised armour. Here, the authors present a chromosome-level reference genome assembly and tissue-specific transcriptomic data for this enigmatic organism.

Nature Communications

220440363

10.1038/S41598-020-67314-W

Group structure and kinship in beluga whale societies

Evolutionary explanations for mammalian sociality typically center on inclusive-fitness benefits of associating and cooperating with close kin, or close maternal kin as in some whale societies, including killer and sperm whales. Their matrilineal structure has strongly influenced the thinking about social structure in less well-studied cetaceans, including beluga whales. In a cross-sectional study of group structure and kinship we found that belugas formed a limited number of distinct group types, consistently observed across populations and habitats. Certain behaviours were associated with group type, but group membership was often dynamic. MtDNA-microsatellite profiling combined with relatedness and network analysis revealed, contrary to predictions, that most social groupings were not predominantly organized around close maternal relatives. They comprised both kin and non-kin, many group members were paternal rather than maternal relatives, and unrelated adult males often traveled together. The evolutionary mechanisms that shape beluga societies are likely complex; fitness benefits may be achieved through reciprocity, mutualism and kin selection. At the largest scales these societies are communities comprising all ages and both sexes where multiple social learning pathways involving kin and non-kin can foster the emergence of cultures. We explore the implications of these findings for species management and the evolution of menopause.

Scientific Reports

220798089

10.1002/ECY.3129

A specialized avian seed dispersal system in a dry-fruited non-photosynthetic plant, Balanophora yakushimensis.

The family Balanophoraceae are among the most unusual of plants because they have aberrant vegetative bodies, highly reduced flowers, and small and reduced embryos (Hansen 1972, Gonzalez et al. 2019). Because the plants lack chlorophyll and are incapable of photosynthesis, they draw nutrition from other organisms. Indeed, like the well-known parasitic plant, Rafflesia, members of the Balanophoraceae acquire both water and nutrients from host plants. They are, therefore, highly specialized root parasites.

Ecology

211100788

10.1002/AJB2.1428

Sexual and natural selection on pollen morphology in Taraxacum.

PREMISE Spiny pollen has evolved independently in multiple entomophilous lineages. Sexual selection may act on exine traits that facilitate male mating success by influencing the transfer of pollen from the anther to the body of the pollinator, while natural selection acts to increase pollen survival. We postulated that relative to sexual congeners, apomictic dandelions undergo relaxed selection on traits associated with male mating success. METHODS We explored sexual selection on exine traits by measuring the propensity for Taraxacum spp. pollen to attach to hairs of flower-visiting bumblebees (Bombus spp.) or flies (Diptera: Syrphidae and Muscoidea) and assessed natural selection by testing whether pollen traits defend against consumption. RESULTS Pollen picked up by bumblebees exhibited a narrower subset of spine-spacing phenotypes, consistent with stabilizing selection. Flies picked up larger pollen from flowers than expected at random. Surveys of corbiculae (pollen basket) contents from foraging bumblebees and feces of flies showed that pollen grains consumed by both kinds of visitors are similar in spine characteristics and size to those produced by the donor. When bees visit inflorescences of apomictic T. officinale, they pick up pollen with spine-spacing phenotypes above the mean and shifted toward those of sexual T. ceratophorum. CONCLUSIONS We demonstrate that traits under sexual selection during pollen pickup vary among pollinators, while natural selection for pollen defense is nil in T. ceratophorum. In hybrid zones between apomictic and sexual dandelions, pollen traits place apomictic donors at a dispersal disadvantage, potentially reinforcing reproductive isolation.

American Journal of Botany

216595925

10.1242/JEB.219287

Reduced immune responsiveness contributes to winter energy conservation in an Arctic bird

ABSTRACT Animals in seasonal environments must prudently manage energy expenditure to survive the winter. This may be achieved through reductions in the allocation of energy for various purposes (e.g. thermoregulation, locomotion, etc.). We studied whether such trade-offs also include suppression of the innate immune response, by subjecting captive male Svalbard ptarmigan (Lagopus muta hyperborea) to bacterial lipopolysaccharide (LPS) during exposure to either mild temperature (0°C) or cold snaps (acute exposure to −20°C), in constant winter darkness when birds were in energy-conserving mode, and in constant daylight in spring. The innate immune response was mostly unaffected by temperature. However, energy expenditure was below baseline when birds were immune challenged in winter, but significantly above baseline in spring. This suggests that the energetic component of the innate immune response was reduced in winter, possibly contributing to energy conservation. Immunological parameters decreased (agglutination, lysis, bacteriostatic capacity) or did not change (haptoglobin/PIT54) after the challenge, and behavioural modifications (anorexia, mass loss) were lengthy (9 days). While we did not study the mechanisms explaining these weak, or slow, responses, it is tempting to speculate they may reflect the consequences of having evolved in an environment where pathogen transmission rate is presumably low for most of the year. This is an important consideration if climate change and increased exploitation of the Arctic would alter pathogen communities at a pace outwith counter-adaption in wildlife. Highlighted Article: Adaptation to the thermally extreme and pathogenically pristine high Arctic may select for year-round energy conservation at the expense of permanently reduced innate immune function.

The Journal of Experimental Biology

220515502

10.1098/RSPB.2020.1147

Self-organization of river vegetation leads to emergent buffering of river flows and water levels

Global climate change is expected to impact hydrodynamic conditions in stream ecosystems. There is limited understanding of how stream ecosystems interact and possibly adapt to novel hydrodynamic conditions. Combining mathematical modelling with field data, we demonstrate that bio-physical feedback between plant growth and flow redistribution triggers spatial self-organization of in-channel vegetation that buffers for changed hydrological conditions. The interplay of vegetation growth and hydrodynamics results in a spatial separation of the stream into densely vegetated, low-flow zones divided by unvegetated channels of higher flow velocities. This self-organization process decouples both local flow velocities and water levels from the forcing effect of changing stream discharge. Field data from two lowland, baseflow-dominated streams support model predictions and highlight two important stream-level emergent properties: vegetation controls flow conveyance in fast-flowing channels throughout the annual growth cycle, and this buffering of discharge variations maintains water depths and wetted habitat for the stream community. Our results provide important evidence of how plant-driven self-organization allows stream ecosystems to adapt to changing hydrological conditions, maintaining suitable hydrodynamic conditions to support high biodiversity.

Proceedings of The Royal Society B: Biological Sciences

32310179

10.1073/PNAS.1703454114

Improved color constancy in honey bees enabled by parallel visual projections from dorsal ocelli

Significance Color sensing requires a capacity to discount the changing color of natural light. We present a biologically validated mathematical solution to this classic problem based on honey bee color vision. The observed spectral tuning of two simple ocellar photoreceptors in the honey bee allows for an optimal color constancy solution to different light environments, including standard CIE (Commission Internationale de l’Eclairage) illuminations, natural forest light, sunlight, or shade. The model is fully supported by a neural pathway potentially allowing for the transfer of spectral information originating from the ocellar photoreceptors to the centralized information processing regions in the brain and explains previously observed behavioral results. This solution to color constancy can be implemented into color imaging systems to enable accurate color interpretation. How can a pollinator, like the honey bee, perceive the same colors on visited flowers, despite continuous and rapid changes in ambient illumination and background color? A hundred years ago, von Kries proposed an elegant solution to this problem, color constancy, which is currently incorporated in many imaging and technological applications. However, empirical evidence on how this method can operate on animal brains remains tenuous. Our mathematical modeling proposes that the observed spectral tuning of simple ocellar photoreceptors in the honey bee allows for the necessary input for an optimal color constancy solution to most natural light environments. The model is fully supported by our detailed description of a neural pathway allowing for the integration of signals originating from the ocellar photoreceptors to the information processing regions in the bee brain. These findings reveal a neural implementation to the classic color constancy problem that can be easily translated into artificial color imaging systems.

Proceedings of the National Academy of Sciences of the United States of America

218620291

10.3390/IJMS21093355

The Protective Role of Bark and Bark Fibers of the Giant Sequoia (Sequoiadendron giganteum) during High-Energy Impacts

The influences of (1) a high fiber content, (2) the arrangement of fibers in fiber groups, and (3) a layered hierarchical composition of the bark of the giant sequoia (Sequoiadendron giganteum) on its energy dissipation capability are analyzed and discussed regarding the relevance for an application in bioinspired components in civil engineering. The giant sequoia is native to the Sierra Nevada (USA), a region with regular rockfalls. It is thus regularly exposed to high-energy impacts, with its bark playing a major protective role, as can be seen in the wild and has been proven in laboratory experiments. The authors quantify the fundamental biomechanical properties of the bark at various length scales, taking into account its hierarchical setup ranging from the integral level (whole bark) down to single bark fibers. Microtensile tests on single fibers and fiber pairs give insights into the properties of single fibers as well as the benefits of the strong longitudinal interconnection between single fibers arranged in pairs. Going beyond the level of single fibers or fiber pairs, towards the integral level, quasistatic compression tests and dynamic impact tests are performed on samples comprising the whole bark (inner and outer bark). These tests elucidate the deformation behavior under quasistatic compression and dynamic impact relevant for the high energy dissipation and impact-damping behavior of the bark. The remarkable energy dissipation capability of the bark at the abovementioned hierarchical levels are linked to the layered and fibrous structure of the bark structurally analyzed by thin sections and SEM and µCT scans.

International Journal of Molecular Sciences

219281945

10.1038/S41586-020-2369-7

IGF1R is an entry receptor for respiratory syncytial virus

Pneumonia resulting from infection is one of the leading causes of death worldwide. Pulmonary infection by the respiratory syncytial virus (RSV) is a large burden on human health, for which there are few therapeutic options 1 . RSV targets ciliated epithelial cells in the airways, but how viruses such as RSV interact with receptors on these cells is not understood. Nucleolin is an entry coreceptor for RSV 2 and also mediates the cellular entry of influenza, the parainfluenza virus, some enteroviruses and the bacterium that causes tularaemia 3 , 4 . Here we show a mechanism of RSV entry into cells in which outside-in signalling, involving binding of the prefusion RSV-F glycoprotein with the insulin-like growth factor-1 receptor, triggers the activation of protein kinase C zeta (PKCζ). This cellular signalling cascade recruits nucleolin from the nuclei of cells to the plasma membrane, where it also binds to RSV-F on virions. We find that inhibiting PKCζ activation prevents the trafficking of nucleolin to RSV particles on airway organoid cultures, and reduces viral replication and pathology in RSV-infected mice. These findings reveal a mechanism of virus entry in which receptor engagement and signal transduction bring the coreceptor to viral particles at the cell surface, and could form the basis of new therapeutics to treat RSV infection. Respiratory syncytial virus enters cells by binding to cell-surface IGFR1, which activates PKCζ and induces trafficking of the NCL coreceptor to the RSV particles at the cell surface.

Nature

214681457

10.1103/PHYSREVLETT.124.105302

Torque and Angular-Momentum Transfer in Merging Rotating Bose-Einstein Condensates.

When rotating classical fluid drops merge together, angular momentum can be advected from one to another due to the viscous shear flow at the drop interface. It remains elusive what the corresponding mechanism is in inviscid quantum fluids such as Bose-Einstein condensates (BECs). Here we report our theoretical study of an initially static BEC merging with a rotating BEC in three-dimensional space along the rotational axis. We show that a solitonlike sheet, resembling a corkscrew, spontaneously emerges at the interface. Rapid angular-momentum transfer at a constant rate universally proportional to the initial angular-momentum density is observed. Strikingly, this transfer does not necessarily involve fluid advection or drifting of the quantized vortices. We reveal that the corkscrew structure can exert a torque that directly creates angular momentum in the static BEC and annihilates angular momentum in the rotating BEC. Uncovering this intriguing angular-momentum transport mechanism may benefit our understanding of various coherent matter-wave systems, spanning from atomtronics on chips to dark matter BECs at cosmic scales.

Physical Review Letters

220517988

10.1073/PNAS.1907360117

Physical limits of flight performance in the heaviest soaring bird

Significance Flapping flight is extremely costly for large birds, yet little is known about the conditions that force them to flap. We attached custom-made “flight recorders” to Andean condors, the world’s heaviest soaring birds, documenting every single wingbeat and when and how individuals gained altitude. Remarkably, condors flapped for only 1% of their flight time, specifically during takeoff and when close to the ground. This is particularly striking as the birds were immature. Thus, our results demonstrate that even inexperienced birds can cover vast distances over land without flapping. Overall, this can help explain how extinct birds with twice the wingspan of condors could have flown. Flight costs are predicted to vary with environmental conditions, and this should ultimately determine the movement capacity and distributions of large soaring birds. Despite this, little is known about how flight effort varies with environmental parameters. We deployed bio-logging devices on the world’s heaviest soaring bird, the Andean condor (Vultur gryphus), to assess the extent to which these birds can operate without resorting to powered flight. Our records of individual wingbeats in >216 h of flight show that condors can sustain soaring across a wide range of wind and thermal conditions, flapping for only 1% of their flight time. This is among the very lowest estimated movement costs in vertebrates. One bird even flew for >5 h without flapping, covering ∼172 km. Overall, > 75% of flapping flight was associated with takeoffs. Movement between weak thermal updrafts at the start of the day also imposed a metabolic cost, with birds flapping toward the end of glides to reach ephemeral thermal updrafts. Nonetheless, the investment required was still remarkably low, and even in winter conditions with weak thermals, condors are only predicted to flap for ∼2 s per kilometer. Therefore, the overall flight effort in the largest soaring birds appears to be constrained by the requirements for takeoff.

Proceedings of the National Academy of Sciences of the United States of America

216593440

10.1242/JEB.219642

Mechanisms and consequences of flight polyphenisms in an outbreaking bark beetle species

ABSTRACT Flight polyphenisms naturally occur as discrete or continuous traits in insects. Discrete flight polyphenisms include winged and wingless morphs, whereas continuous flight polyphenisms can take the form of short- or long-distance fliers. The mountain pine beetle (Dendroctonus ponderosae) exhibits polyphenic variation in flight distance but the consequences of this flight variation on life history strategies of beetles is unknown. This study assessed the effect of flight on two particular aspects of beetle biology: (1) an energetic trade-off between flight distance and host colonisation capacity; and (2) the relationship between flight distance and pheromone production. A 23 h flight treatment was applied to a subset of beetles using computer-linked flight mills. After flight treatment, both flown and unflown (control) beetles were given the opportunity to colonise bolts of host trees, and beetles that entered hosts were aerated to collect pheromone. A trade-off occurred between initiation of host colonisation and percentage body mass lost during flight, which indicates energy use during flight affects host acceptance in female mountain pine beetles. Furthermore, production of the aggregation pheromone trans-verbenol by female beetles was influenced by both percentage body mass lost during flight and flight distance. Male production of exo-brevicomin was affected by beetle condition following flight but not by the energy used during flight. These novel results give new insight into the polyphenic flight behaviour of mountain pine beetles. Flight variation is adaptive by acting to maintain population levels through safe and risky host colonisation strategies. These findings suggest mechanisms that facilitate the extremities of the continuous flight polyphenism spectrum. These opposing mechanisms appear to maintain the high variation in flight exhibited by this species. Highlighted Article: The relationship between energy use during flight and host colonisation in the mountain pine beetle suggests potential selection mechanisms maintaining flight polyphenisms.

The Journal of Experimental Biology

221114305

10.1016/J.CUB.2020.07.046

Pre-extinction Demographic Stability and Genomic Signatures of Adaptation in the Woolly Rhinoceros

Ancient DNA has significantly improved our understanding of the evolution and population history of extinct megafauna. However, few studies have used complete ancient genomes to examine species responses to climate change prior to extinction. The woolly rhinoceros (Coelodonta antiquitatis) was a cold-adapted megaherbivore widely distributed across northern Eurasia during the Late Pleistocene and became extinct approximately 14 thousand years before present (ka BP). While humans and climate change have been proposed as potential causes of extinction [1-3], knowledge is limited on how the woolly rhinoceros was impacted by human arrival and climatic fluctuations [2]. Here, we use one complete nuclear genome and 14 mitogenomes to investigate the demographic history of woolly rhinoceros leading up to its extinction. Unlike other northern megafauna, the effective population size of woolly rhinoceros likely increased at 29.7 ka BP and subsequently remained stable until close to the species' extinction. Analysis of the nuclear genome from a ∼18.5-ka-old specimen did not indicate any increased inbreeding or reduced genetic diversity, suggesting that the population size remained steady for more than 13 ka following the arrival of humans [4]. The population contraction leading to extinction of the woolly rhinoceros may have thus been sudden and mostly driven by rapid warming in the Bølling-Allerød interstadial. Furthermore, we identify woolly rhinoceros-specific adaptations to arctic climate, similar to those of the woolly mammoth. This study highlights how species respond differently to climatic fluctuations and further illustrates the potential of palaeogenomics to study the evolutionary history of extinct species.

Current Biology

11199554

10.1038/NCOMMS14539

Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication

Protein-based biogenic materials provide important inspiration for the development of high-performance polymers. The fibrous mussel byssus, for instance, exhibits exceptional wet adhesion, abrasion resistance, toughness and self-healing capacity–properties that arise from an intricate hierarchical organization formed in minutes from a fluid secretion of over 10 different protein precursors. However, a poor understanding of this dynamic biofabrication process has hindered effective translation of byssus design principles into synthetic materials. Here, we explore mussel byssus assembly in Mytilus edulis using a synergistic combination of histological staining and confocal Raman microspectroscopy, enabling in situ tracking of specific proteins during induced thread formation from soluble precursors to solid fibres. Our findings reveal critical insights into this complex biological manufacturing process, showing that protein precursors spontaneously self-assemble into complex architectures, while maturation proceeds in subsequent regulated steps. Beyond their biological importance, these findings may guide development of advanced materials with biomedical and industrial relevance.

Nature Communications

220389021

10.1088/1748-3190/ABA2F6

School formation characteristics and stimuli based modeling of Tetra fish.

Self-organizing motion is an important yet inadequately understood phenomena in the field of collective behavior. For birds flocks, insect swarms, and fish schools, group behavior can provide a mechanism for defense against predators, better foraging and mating capabilities and increased hydro/aerodynamic efficiency in long-distance migration events. Although collective motion has received much scientific attention, more work is required to model and understand the mechanisms responsible for school initiation and formation, and information transfer within these groups. Here we investigate schooling of Black Tetra (Gymnocorymbus ternetzi) fish triggered by startle stimuli in the form of approaching objects. High-speed video and tagging techniques were used to track the school and individual members. We then measured several variables including reaction times, group formation shapes, fish velocity, group density, and leadership within the group. These data reveal three things: 1) information propagates through the group as a wave, indicating that each fish is not reacting individually to the stimulus, 2) the time taken for information to transfer across the group is independent of group density, and 3) information propagates across large groups faster than would be expected if the fish were simply responding to the motion of their nearest neighbor. A model was then built wherein simulated fish have a simple `stimuli/escape' vector based on a hypothetical field of vision. The model was used to simulate a group of individual fish with initial conditions, size, and stimuli similar to the biological experiments. The model revealed similar behavior to the biological experiments and provide insights into the observed patterns, response times, and wave speeds.

Bioinspiration & Biomimetics

147707295

10.1098/RSBL.2019.0015

Transitive inference in Polistes paper wasps

Transitive inference (TI) is a form of logical reasoning that involves using known relationships to infer unknown relationships (A > B; B > C; then A > C). TI has been found in a wide range of vertebrates but not in insects. Here, we test whether Polistes dominula and Polistes metricus paper wasps can solve a TI problem. Wasps were trained to discriminate between five elements in series (A0B−, B0C−, C0D−, D0E−), then tested on novel, untrained pairs (B versus D). Consistent with TI, wasps chose B more frequently than D. Wasps organized the trained stimuli into an implicit hierarchy and used TI to choose between untrained pairs. Species that form social hierarchies like Polistes may be predisposed to spontaneously organize information along a common underlying dimension. This work contributes to a growing body of evidence that the miniature nervous system of insects does not limit sophisticated behaviours.

Biology Letters

93004099

10.1016/J.CELL.2019.03.029

Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers

Long-range (>10 μm) transport of electrons along networks of Geobacter sulfurreducens protein filaments, known as microbial nanowires, has been invoked to explain a wide range of globally important redox phenomena. These nanowires were previously thought to be type IV pili composed of PilA protein. Here, we report a 3.7 Å resolution cryoelectron microscopy structure, which surprisingly reveals that, rather than PilA, G. sulfurreducens nanowires are assembled by micrometer-long polymerization of the hexaheme cytochrome OmcS, with hemes packed within ∼3.5-6 Å of each other. The inter-subunit interfaces show unique structural elements such as inter-subunit parallel-stacked hemes and axial coordination of heme by histidines from neighboring subunits. Wild-type OmcS filaments show 100-fold greater conductivity than other filaments from a ΔomcS strain, highlighting the importance of OmcS to conductivity in these nanowires. This structure explains the remarkable capacity of soil bacteria to transport electrons to remote electron acceptors for respiration and energy sharing.

Cell

91201667

10.1111/JAV.01972

Flight activity in pallid swifts Apus pallidus during the non-breeding period

Flight activity recorders have recently confirmed that alpine and common swifts spend the majority of their non-breeding period on the wing, which may last 6–10 months. Here we test the hypothesis that the closely related pallid swift, a species with a breeding distribution around the Mediterranean, lead a similar aerial life-style during its migration and wintering periods. The pallid swift usually lays two clutches in one season and therefore spends more time in the breeding area than the common swift. We successfully tracked four pallid swifts with data loggers that record light for geolocation and acceleration every 5 min to monitor flight activity. The birds wintered south of the Sahel in west Africa from the Ivory Coast to Cameroon. The pallid swifts spent the majority of their non-breeding time in flight, especially the first two months after leaving the breeding area in autumn, while a few landing events occurred during the winter. The total time grounded was < 1%, similar to that of the common and alpine swifts. The mass specific flight metabolic rate of swifts is similar to the average non-breeding metabolic rate of a long distance terrestrial migrant, suggesting swifts are not more likely to procure oxidative damage as a consequence of continuous flight than other migrants. The open airspace used by swifts may provide a relatively safe habitat that explain the high survival rate found in swifts.

Journal of Avian Biology

93001738

10.1111/JEB.13446

Sperm head abnormalities are more frequent in songbirds with more helical sperm: A possible trade‐off in sperm evolution

Sperm morphology varies enormously across the animal kingdom. Whilst knowledge of the factors that drive the evolution of interspecific variation in sperm morphology is accumulating, we currently have little understanding of factors that may constrain evolutionary change in sperm traits. We investigated whether susceptibility to sperm abnormalities could represent such a constraint in songbirds, a group characterized by a distinctive helical sperm head shape. Specifically, using 36 songbird species and data from light and scanning electron microscopy, we examined among‐species correlations between the occurrence of sperm head abnormalities and sperm morphology, as well as the correlation between sperm head abnormalities and two indicators of sperm competition. We found that species with more helically shaped sperm heads (i.e., a wider helical membrane and more pronounced cell waveform) had a higher percentage of abnormal sperm heads than species with less helical sperm (i.e., relatively straight sperm) and that sperm head traits were better predictors of head abnormalities than total sperm length. In contrast, there was no correlation between sperm abnormalities and the level of sperm competition. Given that songbird species with more pronounced helical sperm have higher average sperm swimming speed, our results suggest an evolutionary trade‐off between sperm performance and the structural integrity of the sperm head. As such, susceptibility to morphological abnormalities may constrain the evolution of helical sperm morphology in songbirds.

Journal of Evolutionary Biology

73425575

10.1093/JXB/ERZ018

Effects of temperature on the cuticular transpiration barrier of two desert plants with water-spender and water-saver strategies

The efficacy of the cuticular transpiration barrier and its resistance to elevated temperatures are significantly higher in a typical water-saver than in a water-spender plant growing in hot desert.

Journal of Experimental Botany

54600052

10.1017/JFM.2015.513

Wake-induced ‘slaloming’ response explains exquisite sensitivity of seal whisker-like sensors

Blindfolded harbour seals are able to use their uniquely shaped whiskers to track vortex wakes left by moving animals and identify objects that passed by 30 s earlier, an impressive feat, as the flow features have velocities as low as $1~\text{mm}~\text{s}^{-1}$ . The seals sense while swimming, hence their whiskers are sensitive enough to detect small-scale changes in the flow, while rejecting self-generated flow noise. Here we identify and illustrate a novel flow mechanism, causing a large-amplitude ‘slaloming’ whisker response, which allows artificial whiskers with the identical unique undulatory geometry as those of the harbour seal to detect the features of minute flow fluctuations when placed within wakes. Whereas in open water the whisker responds with very low-amplitude vibration, once within a wake, it oscillates with large amplitude and, importantly, its response frequency coincides with the Strouhal frequency of the upstream cylinder, making the detection of an upstream wake and an estimation of the size and shape of the wake-generating body possible. This mechanism has some similarities with the flow mechanisms observed in actively controlled propulsive foils within upstream wakes and trout swimming behind bluff cylinders in a stream, but there are also differences caused by the unique whisker morphology, which enables it to respond passively and within a much wider parametric range.

Journal of Fluid Mechanics

73419742

10.1021/ACS.JPCLETT.8B03719

Contrasting Behavior of Antifreeze Proteins: Ice Growth Inhibitors and Ice Nucleation Promoters.

Several types of natural molecules interact specifically with ice crystals. Small antifreeze proteins (AFPs) adsorb to particular facets of ice crystals, thus inhibiting their growth, whereas larger ice-nucleating proteins (INPs) can trigger the formation of new ice crystals at temperatures much higher than the homogeneous ice nucleation temperature of pure water. It has been proposed that both types of proteins interact similarly with ice and that, in principle, they may be able to exhibit both functions. Here we investigated two naturally occurring antifreeze proteins, one from fish, type-III AFP, and one from beetles, TmAFP. We show that in addition to ice growth inhibition, both can also trigger ice nucleation above the homogeneous freezing temperature, providing unambiguous experimental proof for their contrasting behavior. Our analysis suggests that the predominant difference between AFPs and INPs is their molecular size, which is a very good predictor of their ice nucleation temperature.

Journal of Physical Chemistry Letters

104318447

10.1016/J.JPOWSOUR.2019.01.027

In situ enrichment of microbial communities on polarized electrodes deployed in alkaline hot springs

Abstract The discovery of the ability of microorganisms to exchange electrons with inert electrodes has triggered new areas in fundamental and applied research. However, the field is currently limited to several known electrochemically active microorganisms enriched and isolated in research laboratories. An alternative strategy is to enrich such microorganisms in their native environment by allowing them to exchange electrons with polarized solid electrodes. The use of this approach is currently limited because of a lack of available tools. We developed a low-cost, battery-operated potentiostat that is capable of controlling the potential of a working electrode and can be deployed and operated remotely, allowing the enrichment of microorganisms on electrodes in their native environment. The device was tested in four alkaline hot springs in Heart Lake Geyser Basin in Yellowstone National Park (with a temperature ranging from 45 οC to 91 οC and a relatively constant pH of 8.5–8.7). Microbial community analysis showed a change in microbial community structure after 32 days of polarization. The impact of polarization on microbial community was most substantial on the electrodes that generated the highest cathodic and anodic currents, suggesting a direct impact of polarization on electrode microbial community.

Journal of Power Sources

206151975

10.1098/RSIF.2017.0901

Gyroscopic stabilization minimizes drag on Ruellia ciliatiflora seeds

Fruits of Ruellia ciliatiflora (Acanthaceae) explosively launch small (2.5 mm diameter × 0.46 mm thick), disc-shaped seeds at velocities over 15 m s−1, reaching distances of up to 7 m. Through high-speed video analysis, we observe that seeds fly with extraordinary backspin of up to 1660 Hz. By modelling the seeds as spinning discs, we show that flying with backspin is stable against gyroscopic precession. This stable backspin orientation minimizes the frontal area during flight, decreasing drag force on the seeds and thus increasing dispersal distance. From high-speed video of the seeds' flight, we experimentally determine drag forces that are 40% less than those calculated for a sphere of the same volume and density. This reduces the energy costs for seed dispersal by up to a factor of five.

Journal of the Royal Society Interface

91396327

10.1098/RSIF.2018.0561

Collective ventilation in honeybee nests

European honey bees (Apis mellifera) live in large congested nest cavities with a single opening that limits passive ventilation. When the local air temperature exceeds a threshold, the nests are actively ventilated by bees fanning their wings at the nest entrance. Here, we show that colonies with relatively large nest entrances use an emergent ventilation strategy where fanning bees self-organize to form groups, separating regions of continuous inflow and outflow. The observed spatio-temporal patterns correlate the air velocity and air temperature along the entrances to the distribution of fanning bees. A mathematical model that couples these variables to known fanning behaviour of individuals recapitulates their collective dynamics. Additionally, the model makes predictions about the temporal stability of the fanning group as a function of the temperature difference between the environment and the nest. Consistent with these predictions, we observe that the fanning groups drift, cling to the entrance boundaries, break-up and reform as the ambient temperature varies over a period of days. Overall, our study shows how honeybees use flow-mediated communication to self-organize into a steady state in fluctuating environments.

Journal of the Royal Society Interface

73456003

10.1111/MEC.15022

Phototactic tails: Evolution and molecular basis of a novel sensory trait in sea snakes

Dermal phototaxis has been reported in a few aquatic vertebrate lineages spanning fish, amphibians and reptiles. These taxa respond to light on the skin of their elongate hind‐bodies and tails by withdrawing under cover to avoid detection by predators. Here, we investigated tail phototaxis in sea snakes (Hydrophiinae), the only reptiles reported to exhibit this sensory behaviour. We conducted behavioural tests in 17 wild‐caught sea snakes of eight species by illuminating the dorsal surface of the tail and midbody skin using cold white, violet, blue, green and red light. Our results confirmed phototactic tail withdrawal in the previously studied Aipysurus laevis, revealed this trait for the first time in A. duboisii and A. tenuis, and suggested that tail photoreceptors have peak spectral sensitivities between blue and green light (457–514 nm). Based on these results, and an absence of photoresponses in five Aipysurus and Hydrophis species, we tentatively infer that tail phototaxis evolved in the ancestor of a clade of six Aipysurus species (comprising 10% of all sea snakes). Quantifying tail damage, we found that the probability of sustaining tail injuries was not influenced by tail phototactic ability in snakes. Gene profiling showed that transcriptomes of both tail skin and body skin lacked visual opsins but contained melanopsin (opn4x) in addition to key genes of the retinal regeneration and phototransduction cascades. This work suggests that a nonvisual photoreceptor (e.g., Gq rhabdomeric) signalling pathway underlies tail phototaxis, and provides candidate gene targets for future studies of this unusual sensory innovation in reptiles.

Molecular Ecology

220541911

10.1038/S41586-020-2468-5

Bacterial chemolithoautotrophy via manganese oxidation

Manganese is one of the most abundant elements on Earth. The oxidation of manganese has long been theorized1—yet has not been demonstrated2–4—to fuel the growth of chemolithoautotrophic microorganisms. Here we refine an enrichment culture that exhibits exponential growth dependent on Mn(II) oxidation to a co-culture of two microbial species. Oxidation required viable bacteria at permissive temperatures, which resulted in the generation of small nodules of manganese oxide with which the cells associated. The majority member of the culture—which we designate ‘Candidatus Manganitrophus noduliformans’—is affiliated to the phylum Nitrospirae (also known as Nitrospirota), but is distantly related to known species of Nitrospira and Leptospirillum. We isolated the minority member, a betaproteobacterium that does not oxidize Mn(II) alone, and designate it Ramlibacter lithotrophicus. Stable-isotope probing revealed 13CO2 fixation into cellular biomass that was dependent upon Mn(II) oxidation. Transcriptomic analysis revealed candidate pathways for coupling extracellular manganese oxidation to aerobic energy conservation and autotrophic CO2 fixation. These findings expand the known diversity of inorganic metabolisms that support life, and complete a biogeochemical energy cycle for manganese5,6 that may interface with other major global elemental cycles. A co-culture of two newly identified microorganisms—‘Candidatus Manganitrophus noduliformans’ and Ramlibacter lithotrophicus—exhibits exponential growth that is dependent on manganese(II) oxidation, demonstrating the viability of this metabolism for supporting life.

Nature

139103824

10.1038/S41467-019-09814-6

Unique structural features of a bacterial autotransporter adhesin suggest mechanisms for interaction with host macromolecules

Autotransporters are the largest family of outer membrane and secreted proteins in Gram-negative bacteria. Most autotransporters are localised to the bacterial surface where they promote colonisation of host epithelial surfaces. Here we present the crystal structure of UpaB, an autotransporter that is known to contribute to uropathogenic E. coli (UPEC) colonisation of the urinary tract. We provide evidence that UpaB can interact with glycosaminoglycans and host fibronectin. Unique modifications to its core β-helical structure create a groove on one side of the protein for interaction with glycosaminoglycans, while the opposite face can bind fibronectin. Our findings reveal far greater diversity in the autotransporter β-helix than previously thought, and suggest that this domain can interact with host macromolecules. The relevance of these interactions during infection remains unclear.Autotransporter proteins are localised to the bacterial surface and promote colonisation of host epithelial surfaces. Here, the authors present the crystal structure of autotransporter UpaB and show evidence for distinct binding sites for glycosaminoglycans and host fibronectin.

Nature Communications

16214504

10.1007/BF00384487

The central role of Clark's nutcracker in the dispersal and establishment of whitebark pine

SummaryWhitebark pine (Pinus albicaulis) is known to have its seeds harvested and cached in the soil by Clark's Nutcracker (Nucifraga columbiana), and unretrieved seeds are known to be capable of germinating and establishing new pines. Many other vertebrates also harvest and feed on these seeds, however, and the roles of these animals as dispersers and establishers of whitebark pine has been uncertain. This work demonstrates that birds other than the nutcracker, rodents, and other mammals do not have the requisite behaviors to systematically disperse or establish whitebark pine, and that the pine is therefore dependent on the nutcracker for its regeneration. These findings support previous suggestions that Clark's Nutcracker is a specialized frugivore that has profoundly influenced the ecology and the evolution of whitebark pine.

Oecologia

204244045

10.1371/JOURNAL.PBIO.3000427

Shaping of a three-dimensional carnivorous trap through modulation of a planar growth mechanism

Leaves display a remarkable range of forms, from flat sheets with simple outlines to cup-shaped traps. Although much progress has been made in understanding the mechanisms of planar leaf development, it is unclear whether similar or distinctive mechanisms underlie shape transformations during development of more complex curved forms. Here, we use 3D imaging and cellular and clonal analysis, combined with computational modelling, to analyse the development of cup-shaped traps of the carnivorous plant Utricularia gibba. We show that the transformation from a near-spherical form at early developmental stages to an oblate spheroid with a straightened ventral midline in the mature form can be accounted for by spatial variations in rates and orientations of growth. Different hypotheses regarding spatiotemporal control predict distinct patterns of cell shape and size, which were tested experimentally by quantifying cellular and clonal anisotropy. We propose that orientations of growth are specified by a proximodistal polarity field, similar to that hypothesised to account for Arabidopsis leaf development, except that in Utricularia, the field propagates through a highly curved tissue sheet. Independent evidence for the polarity field is provided by the orientation of glandular hairs on the inner surface of the trap. Taken together, our results show that morphogenesis of complex 3D leaf shapes can be accounted for by similar mechanisms to those for planar leaves, suggesting that simple modulations of a common growth framework underlie the shaping of a diverse range of morphologies.

PLOS Biology

85544267

10.1371/JOURNAL.PBIO.3000057

A small proportion of Talin molecules transmit forces at developing muscle attachments in vivo

Cells in developing organisms are subjected to particular mechanical forces that shape tissues and instruct cell fate decisions. How these forces are sensed and transmitted at the molecular level is therefore an important question, one that has mainly been investigated in cultured cells in vitro. Here, we elucidate how mechanical forces are transmitted in an intact organism. We studied Drosophila muscle attachment sites, which experience high mechanical forces during development and require integrin-mediated adhesion for stable attachment to tendons. Therefore, we quantified molecular forces across the essential integrin-binding protein Talin, which links integrin to the actin cytoskeleton. Generating flies expressing 3 Förster resonance energy transfer (FRET)-based Talin tension sensors reporting different force levels between 1 and 11 piconewton (pN) enabled us to quantify physiologically relevant molecular forces. By measuring primary Drosophila muscle cells, we demonstrate that Drosophila Talin experiences mechanical forces in cell culture that are similar to those previously reported for Talin in mammalian cell lines. However, in vivo force measurements at developing flight muscle attachment sites revealed that average forces across Talin are comparatively low and decrease even further while attachments mature and tissue-level tension remains high. Concomitantly, the Talin concentration at attachment sites increases 5-fold as quantified by fluorescence correlation spectroscopy (FCS), suggesting that only a small proportion of Talin molecules are mechanically engaged at any given time. Reducing Talin levels at late stages of muscle development results in muscle–tendon rupture in the adult fly, likely as a result of active muscle contractions. We therefore propose that a large pool of adhesion molecules is required to share high tissue forces. As a result, less than 15% of the molecules experience detectable forces at developing muscle attachment sites at the same time. Our findings define an important new concept of how cells can adapt to changes in tissue mechanics to prevent mechanical failure in vivo.

PLOS Biology

25465608

10.1073/PNAS.1714874114

Superhydrophobic diving flies (Ephydra hians) and the hypersaline waters of Mono Lake

Significance Superhydrophobic surfaces have been of key academic and commercial interest since the discovery of the so-called lotus effect in 1977. The effect of different ions on complex superhydrophobic biological systems, however, has received little attention. By bringing together ecology, biomechanics, physics, and chemistry our study provides insight into the ion-specific effects of wetting in the presence of sodium carbonate and its large-scale consequences. By comparing the surface structure and chemistry of the alkali fly—an important food source for migrating birds—to other species we show that their uniquely hydrophobic properties arise from very small physical and chemical changes, thereby connecting picoscale physics with globally important ecological impacts. The remarkable alkali fly, Ephydra hians, deliberately crawls into the alkaline waters of Mono Lake to feed and lay eggs. These diving flies are protected by an air bubble that forms around their superhydrophobic cuticle upon entering the lake. To study the physical mechanisms underlying this process we measured the work required for flies to enter and leave various aqueous solutions. Our measurements show that it is more difficult for the flies to escape from Mono Lake water than from fresh water, due to the high concentration of Na2CO3 which causes water to penetrate and thus wet their setose cuticle. Other less kosmotropic salts do not have this effect, suggesting that the phenomenon is governed by Hofmeister effects as well as specific interactions between ion pairs. These effects likely create a small negative charge at the air–water interface, generating an electric double layer that facilitates wetting. Compared with six other species of flies, alkali flies are better able to resist wetting in a 0.5 M Na2CO3 solution. This trait arises from a combination of factors including a denser layer of setae on their cuticle and the prevalence of smaller cuticular hydrocarbons compared with other species. Although superbly adapted to resisting wetting, alkali flies are vulnerable to getting stuck in natural and artificial oils, including dimethicone, a common ingredient in sunscreen and other cosmetics. Mono Lake’s alkali flies are a compelling example of how the evolution of picoscale physical and chemical changes can allow an animal to occupy an entirely new ecological niche.

Proceedings of the National Academy of Sciences of the United States of America

76660652

10.1073/PNAS.1815394116

Synergy of topoisomerase and structural-maintenance-of-chromosomes proteins creates a universal pathway to simplify genome topology

Significance Vital biological processes such as gene transcription and cell division may be severely impaired by inevitable entanglements ensuing from the extreme length and confinement of the genome. The family of topoisomerase proteins has independently evolved in different organisms to resolve these topological problems, yet no existing model can explain how topoisomerase alone can reduce the topological complexity of DNA in vivo. We propose that a synergistic mechanism between topoisomerase and a family of slip-link–like proteins called structural maintenance of chromosomes (SMC) can provide a pathway to systematically resolve topological entanglements even under physiological crowding and confinement. Given the ubiquity of topoisomerase and SMC, we argue that the uncovered mechanism is at work throughout the cell cycle and across different organisms. Topological entanglements severely interfere with important biological processes. For this reason, genomes must be kept unknotted and unlinked during most of a cell cycle. Type II topoisomerase (TopoII) enzymes play an important role in this process but the precise mechanisms yielding systematic disentanglement of DNA in vivo are not clear. Here we report computational evidence that structural-maintenance-of-chromosomes (SMC) proteins—such as cohesins and condensins—can cooperate with TopoII to establish a synergistic mechanism to resolve topological entanglements. SMC-driven loop extrusion (or diffusion) induces the spatial localization of essential crossings, in turn catalyzing the simplification of knots and links by TopoII enzymes even in crowded and confined conditions. The mechanism we uncover is universal in that it does not qualitatively depend on the specific substrate, whether DNA or chromatin, or on SMC processivity; we thus argue that this synergy may be at work across organisms and throughout the cell cycle.

Proceedings of the National Academy of Sciences of the United States of America

1427069

10.1098/RSPB.2007.1188

Geometry and self-righting of turtles

Terrestrial animals with rigid shells face imminent danger when turned upside down. A rich variety of righting strategies of beetle and turtle species have been described, but the exact role of the shell's geometry in righting is so far unknown. These strategies are often based on active mechanisms, e.g. most beetles self-right via motion of their legs or wings; flat, aquatic turtles use their muscular neck to flip back. On the other hand, highly domed, terrestrial turtles with short limbs and necks have virtually no active control: here shape itself may serve as a fundamental tool. Based on field data gathered on a broad spectrum of aquatic and terrestrial turtle species we develop a geometric model of the shell. Inspired by recent mathematical results, we demonstrate that a simple mechanical classification of the model is closely linked to the animals' righting strategy. Specifically, we show that the exact geometry of highly domed terrestrial species is close to optimal for self-righting, and the shell's shape is the predominant factor of their ability to flip back. Our study illustrates how evolution solved a far-from-trivial geometrical problem and equipped some turtles with monostatic shells: beautiful forms, which rarely appear in nature otherwise.

Proceedings of The Royal Society B: Biological Sciences

69172916

10.1126/SCIADV.AAU9183

Spider dragline silk as torsional actuator driven by humidity

Spider dragline silk exhibits a self-powered torsion actuation driven by humidity, potentially acting as a novel torsional actuator. Self-powered actuation driven by ambient humidity is of practical interest for applications such as hygroscopic artificial muscles. We demonstrate that spider dragline silk exhibits a humidity-induced torsional deformation of more than 300°/mm. When the relative humidity reaches a threshold of about 70%, the dragline silk starts to generate a large twist deformation independent of spider species. The torsional actuation can be precisely controlled by regulating the relative humidity. The behavior of humidity-induced twist is related to the supercontraction behavior of spider dragline silk. Specifically, molecular simulations of MaSp1 and MaSp2 proteins in dragline silk reveal that the unique torsional property originates from the presence of proline in MaSp2. The large proline rings also contribute to steric exclusion and disruption of hydrogen bonding in the molecule. This property of dragline silk and its structural origin can inspire novel design of torsional actuators or artificial muscles and enable the development of designer biomaterials.

Science Advances

182953012

10.1137/19M1262322

Detecting a Prey in a Spider Orb Web

We consider the inverse problem of localizing a prey hitting a spider orb-web from dynamic measurements taken near the center of the web, where the spider is supposed to stay. The actual discrete orb-web, formed by a finite number of radial and circumferential threads, is modelled as a continuous membrane. The membrane has a specific fibrous structure, which is inherited from the original discrete web, and it is subject to tensile pre-stress in the referential configuration. The transverse load describing the prey's impact is assumed of the form $g(t)f(x)$, where $g(t)$ is a known function of time and $f(x)$ is the unknown term depending on the position variable $x$. For axially-symmetric orb-webs supported at the boundary and undergoing infinitesimal transverse deformations, we prove a uniqueness result for $f(x)$ in terms of measurements of the transverse dynamic displacement taken on an arbitrarily small and thin ring centered at the origin of the web, for a sufficiently large interval of time.

Siam Journal on Applied Mathematics

128360674

10.1140/EPJE/I2019-11812-1

Type-I collagen fibrils: From growth morphology to local order

Abstract.The length of type-I collagen fibrils in solution increases through the development and progress of pointed tips appearing successively at the two ends of an axis-symmetric shaft with constant diameter. Those tips, respectively fine ($\alpha$α) or coarse ($ \beta$β) have opposite molecular orientations. The $\alpha$α-pointed tips, the first to appear, are particularly remarkable as they all show, on most of their length, a common parabolic profile which stays constant during the growth. Assuming that the latter occurs by lateral accretion of individual molecules in staggered configuration, we propose to give account of this prominent morphological feature along a purely geometrical argument, the profile of a tip being linked to the shape of the trajectories followed all along the accretion process. Among several possible trajectories, Fermat spirals lead to a parabolic profile in perfect agreement with the one observed for $\alpha$α-pointed tips. This is to be put in relation with the presence of such spirals in phyllotactic patterns which ensure the best packing efficiency in cases of axis-symmetry, which is indeed that of dense collagen fibrils. Moreover, those patterns are structured by concentric circles of dislocations, constitutive of the structure itself, whose behaviour might contribute to the mechanical properties of the fibrils.Graphical abstract

European Physical Journal E

225067159

10.1140/EPJST/E2020-900273-X

Delay of ice formation on penguin feathers

Cold-weather penguins continually dive in and out of the water and get splashed by waves during the frigid Antarctic winter. Yet, even under these extreme sub-zero conditions, macroscopic ice crystals are typically not observed on their feathers. In this work, we hypothesize that the origin of the anti-icing properties of a cold-weather penguin’s feathers comes from a unique combination of the feather’s macroscopic structure, the nanoscale topography of its barbules, and the hydrophobicity of its preen oil. We show that, the combination of all three, make cold-weather penguin feathers both highly water repellant and icephobic. In this paper, we present the results from a series of droplet freezing experiments performed on feathers from a number of species of both cold-weather and warm-weather penguins. Compared to a smooth glass substrate, freezing was delayed by a factor of 30-times for drops deposited on warm-weather penguin feathers and 60-times for cold-weather penguins. The difference in freezing time between warm- and cold-weather penguins was statistically significant and can be attributed to the increase in the contact angle measured between the drop and the feather of the cold-weather penguin. This increased contact angle is the result of an increase in the hydrophobicity of the preen oil and the inclusion of nanoscale, air-trapping dimples on the surface of the barbules. The physics of this delay are explained through the development of a simple heat transfer model which demonstrates that increasing contact angle is a primary cause of increased freezing time and icephobicity. The results of this study can be used to motivate the designs of biomimetic surfaces to minimize ice formation in extreme conditions for a number of important engineering applications.

European Physical Journal-special Topics

224914667

10.1039/D0EE01281E

Copper-bottomed: electrochemically active bacteria exploit conductive sulphide networks for enhanced electrogeneity

In this study, we demonstrate that anodic electroactive bacteria like Geobacter sulfurreducens generate copper(I) and copper(II) sulphides when grown on copper electrodes. The insoluble copper sulphides form a conductive network within the biofilms, strongly enhancing the biofilm electrogeneity – i.e., the ability of the biofilm to produce electric currents. Compared to biofilms grown on graphite, the average relative current density of copper-based biofilms was 237%, with a maximum geometric current density of 1.59 ± 0.23 mA cm−2. An additional electrochemical CuS deposition prior to biofilm cultivation further increased the bioelectrocatalytic current generation to 2 mA cm−2. The chemical deposition of CuS onto graphite allowed cultivating biofilms with current densities 134% higher than at unmodified graphite. This approach – the chemical CuS deposition onto inexpensive electrode materials – thus represents a promising pathway for the development of scalable, high-performance electrode materials for microbial electrochemical technologies.

Energy and Environmental Science

3658414

10.1007/S11104-017-3539-8

Nickel hyperaccumulation mechanisms: a review on the current state of knowledge

BackgroundHyperaccumulator plants are unusual plants that accumulate particular metals or metalloids, such as nickel, zinc, cadmium and arsenic, in their living tissues to concentrations that are hundreds to thousands of times greater than what is normal for most plants. The hyperaccumulation phenomenon is rare (exhibited by less than 0.2% of all angiosperms), with most of the ~500 hyperaccumulator species known globally for nickel.ScopeThis review highlights the contemporary understanding of nickel hyperaccumulation processes, which include root uptake and sequestration, xylem loading and transport, leaf compartmentation and phloem translocation processes.ConclusionsHyperaccumulator plants have evolved highly efficient physiological mechanisms for taking up nickel in their roots followed by rapid translocation and sequestration into the aerial shoots. The uptake of nickel is mainly involved with low affinity transport systems, presumably from the ZIP family. The presence of high concentrations of histidine prevents nickel sequestration in roots. Nickel is efficiently loaded into the xylem, where it mainly presents as Ni2+. The leaf is the main storage organ, which sequestrates nickel in non-active sites, e.g. vacuoles and apoplast. Recent studies show that phloem translocates high levels of nickel, which has a strong impact on nickel accumulation in young growing tissues.

Plant and Soil

220504003

10.1038/S41567-020-0930-9

Universal elastic mechanism for stinger design

Living organisms use stingers that vary in length L over eight orders of magnitude, from a few tens of nanometres to several metres, across a wide array of biological taxa. Despite the extreme variation in size, their structures are strikingly similar. However, the mechanism responsible for this remarkable morphological convergence remains unknown. Using basic physical arguments and biomimetic experiments, we reveal an optimal design strategy that links their length, base diameter d 0 , Young’s modulus E and friction force per unit area μ p 0 . This principle can be framed simply as $${d}_{0} \approx {(\mu {p}_{0}/E)}^{1/3}L$$ d 0 ≈ ( μ p 0 / E ) 1 / 3 L . Existing data from measurements on viruses, algae, marine invertebrates, terrestrial invertebrates, plants, terrestrial vertebrates, marine vertebrates—as well as man-made objects such as nails, needles and weapons—are consistent with our predictions. Our results highlight the evolutionary adaptation of mechanical traits to the constraints imposed by friction, elastic stability and cost. The structures of stingers of living organisms are surprisingly similar despite their vastly different lengths. Now, stingers are found to obey a unifying mechanistic principle that characterizes the stingers resistance to buckling.

Nature Physics

220601220

10.1126/SCIADV.ABB2307

Compact nanoscale textures reduce contact time of bouncing droplets

Compact nanoscale textures reduce contact time of bouncing droplets with implications in insect survival and miniature drones. Many natural surfaces are capable of rapidly shedding water droplets—a phenomenon that has been attributed to the presence of low solid fraction textures (Φs ~ 0.01). However, recent observations revealed the presence of unusually high solid fraction nanoscale textures (Φs ~ 0.25 to 0.64) on water-repellent insect surfaces, which cannot be explained by existing wetting theories. Here, we show that the contact time of bouncing droplets on high solid fraction surfaces can be reduced by reducing the texture size to ~100 nm. We demonstrated that the texture size–dependent contact time reduction could be attributed to the dominance of line tension on nanotextures and that compact arrangement of nanotextures is essential to withstand the impact pressure of raindrops. Our findings illustrate a potential survival strategy of insects to rapidly shed impacting raindrops, and suggest a previously unidentified design principle to engineering robust water-repellent materials for applications including miniaturized drones.

Science Advances

225481382

10.1002/ESP.4933

A seismic monitoring approach to detect and quantify river sediment mobilization by steelhead redd‐building activity

The role of spawning salmonids in altering river bed morphology and sediment transport is significant, yet poorly understood. This is due, in large part, to limitations in monitoring the redd‐build ...

Earth Surface Processes and Landforms

225666691

10.1038/S41567-020-0935-4

Undulation enables gliding in flying snakes

When flying snakes glide, they use aerial undulation. To determine if aerial undulation is a flight control strategy or a non-functional behavioural vestige of lateral undulation, we measured snake glides using high-speed motion capture and developed a new dynamical model of gliding. Reconstructions of the snake’s wing-body reveal that aerial undulation is composed of horizontal and vertical waves, whose phases differ by 90° and whose frequencies differ by a factor of two. Using these results, we developed a three-dimensional mathematical model of snake flight that incorporates aerodynamic and inertial effects. Although simulated glides without undulation attained some horizontal distance, they are biologically unrealistic because they failed due to roll and pitch instabilities. In contrast, the inclusion of undulation stabilized the rotational motion and markedly increased glide performance. This work demonstrates that aerial undulation in snakes serves a different function than known uses of undulation in other animals, and suggests a new template of control for dynamic flying robots. Observations of flying snakes inform the development of a dynamical model of gliding taking undulation into account. This work suggests that aerial undulation has a different function in snakes than in other animals.

Nature Physics

173992087

10.1016/J.CUB.2019.03.035

Social immunity in insects

When animals become sick, infected cells and an armada of activated immune cells attempt to eliminate the pathogen from the body. Once infectious particles have breached the body's physical barriers of the skin or gut lining, an initially local response quickly escalates into a systemic response, attracting mobile immune cells to the site of infection. These cells complement the initial, unspecific defense with a more specialized, targeted response. This can also provide long-term immune memory and protection against future infection. The cell-autonomous defenses of the infected cells are thus aided by the actions of recruited immune cells. These specialized cells are the most mobile cells in the body, constantly patrolling through the otherwise static tissue to detect incoming pathogens. Such constant immune surveillance means infections are noticed immediately and can be rapidly cleared from the body. Some immune cells also remove infected cells that have succumbed to infection. All this prevents pathogen replication and spread to healthy tissues. Although this may involve the sacrifice of some somatic tissue, this is typically replaced quickly. Particular care is, however, given to the reproductive organs, which should always remain disease free (immune privilege).

Current Biology

19076292

10.1073/PNAS.1620612114

Investigation of hindwing folding in ladybird beetles by artificial elytron transplantation and microcomputed tomography

Significance Hindwings in ladybird beetles successfully achieve compatibility between the deformability (instability) required for wing folding and strength property (stability) required for flying. This study demonstrates how ladybird beetles address these two conflicting requirements by an unprecedented technique using artificial wings. Our results, which clarify the detailed wing-folding process and reveal the supporting structures, provide indispensable initial knowledge for revealing this naturally evolved optimization system. Investigating the characteristics in the venations and crease patterns revealed in this study could provide an innovative designing method, enabling the integration of structural stability and deformability, and thus could have a considerable impact on engineering science. Ladybird beetles are high-mobility insects and explore broad areas by switching between walking and flying. Their excellent wing transformation systems enabling this lifestyle are expected to provide large potential for engineering applications. However, the mechanism behind the folding of their hindwings remains unclear. The reason is that ladybird beetles close the elytra ahead of wing folding, preventing the observation of detailed processes occurring under the elytra. In the present study, artificial transparent elytra were transplanted on living ladybird beetles, thereby enabling us to observe the detailed wing-folding processes. The result revealed that in addition to the abdominal movements mentioned in previous studies, the edge and ventral surface of the elytra, as well as characteristic shaped veins, play important roles in wing folding. The structures of the wing frames enabling this folding process and detailed 3D shape of the hindwing were investigated using microcomputed tomography. The results showed that the tape spring-like elastic frame plays an important role in the wing transformation mechanism. Compared with other beetles, hindwings in ladybird beetles are characterized by two seemingly incompatible properties: (i) the wing rigidity with relatively thick veins and (ii) the compactness in stored shapes with complex crease patterns. The detailed wing-folding process revealed in this study is expected to facilitate understanding of the naturally optimized system in this excellent deployable structure.

Proceedings of the National Academy of Sciences of the United States of America

214734064

10.1093/AOB/MCAA058

Pollen adaptation to ant pollination: a case study from the Proteaceae

Abstract Background and Aims Ant–plant associations are widely diverse and distributed throughout the world, leading to antagonistic and/or mutualistic interactions. Ant pollination is a rare mutualistic association and reports of ants as effective pollinators are limited to a few studies. Conospermum (Proteaceae) is an insect-pollinated genus well represented in the south-western Australia biodiversity hotspot, and here we aimed to evaluate the role of ants as pollinators of C. undulatum. Methods Pollen germination after contact with several species of ants and bees was tested for C. undulatum and five co-flowering species for comparison. We then sampled the pollen load of floral visitors of C. undulatum to assess whether ants carried a pollen load sufficient to enable pollination. Lastly, we performed exclusion treatments to assess the relative effect of flying- and non-flying-invertebrate floral visitors on the reproduction of C. undulatum. For this, we measured the seed set under different conditions: ants exclusion, flying-insects exclusion and control. Key Results Pollen of C. undulatum, along with the other Conospermum species, had a germination rate after contact with ants of ~80 % which did not differ from the effect of bees; in contrast, the other plant species tested showed a drop in the germination rate to ~10 % following ant treatments. Although ants were generalist visitors, they carried a pollen load with 68–86 % of suitable grains. Moreover, ants significantly contributed to the seed set of C. undulatum. Conclusions Our study highlights the complexity of ant–flower interactions and suggests that generalizations neglecting the importance of ants as pollinators cannot be made. Conospermum undulatum has evolved pollen with resistance to the negative effect of ant secretions on pollen grains, with ants providing effective pollination services to this threatened species.

Annals of Botany

218552030

10.1126/SCIENCE.ABB0064

Drones become even more insect-like

Mosquitoes' exceptional sensitivity to sound and airflow inspires new collision avoidance technology Evolutionary pressures in the animal kingdom have, over the course of several hundred million years, produced a diverse array of creatures highly adapted to survival within their own niche environments. Such adaptations coincide with optimized and efficient materials, body structure, and behavior. Humans have long drawn inspiration from nature in the creation of new technologies—for example, the earliest attempts at flight based on emulation of birds—and many benefits stem from the study of processes, materials, methods, and organizational structures of living organisms. On page 634 of this issue, Nakata et al. (1) exemplify the bioinspired design methodology through their investigation of the sound- and airflow-sensing capabilities of the southern house mosquito Culex quinquefasciatus and subsequent creation of a small quad-copter drone with an autonomous collision avoidance system based on the same sensing principles. The sensor displays compelling advantages in weight, power, and deployability over existing technology.

Science

216588642

10.1098/RSPB.2020.0457

Deciphering an extreme morphology: bone microarchitecture of the hero shrew backbone (Soricidae: Scutisorex)

Biological structures with extreme morphologies are puzzling because they often lack obvious functions and stymie comparisons to homologous or analogous features with more typical shapes. An example of such an extreme morphotype is the uniquely modified vertebral column of the hero shrew Scutisorex, which features numerous accessory intervertebral articulations and massively expanded transverse processes. The function of these vertebral structures is unknown, and it is difficult to meaningfully compare them to vertebrae from animals with known behavioural patterns and spinal adaptations. Here, we use trabecular bone architecture of vertebral centra and quantitative external vertebral morphology to elucidate the forces that may act on the spine of Scutisorex and that of another large shrew with unmodified vertebrae (Crocidura goliath). X-ray micro-computed tomography (µCT) scans of thoracolumbar columns show that Scutisorex thori is structurally intermediate between C. goliath and S. somereni internally and externally, and both Scutisorex species exhibit trabecular bone characteristics indicative of higher in vivo axial compressive loads than C. goliath. Under compressive load, Scutisorex vertebral morphology is adapted to largely restrict bending to the sagittal plane (flexion). Although these findings do not solve the mystery of how Scutisorex uses its byzantine spine in vivo, our work suggests potentially fruitful new avenues of investigation for learning more about the function of this perplexing structure.

Proceedings of The Royal Society B: Biological Sciences

114210102

10.1017/S0368393100109915

The Silent Flight of Owls

It is possible to trace, in the flying equipment of birds, feathered versions of many of the refinements that render the modern aeroplane more efficient than its predecessors. It would, therefore, be a mistake to ignore birds as a guide to possible future developments. One of the most interesting groups of birds is that which includes all the owls, for there is a possible connection between the manner in which their strikingly silent flight is achieved and the increasingly pressing problem of silencing airscrews.

221205501

10.1101/2020.08.08.238469

An ultra-potent synthetic nanobody neutralizes SARS-CoV-2 by locking Spike into an inactive conformation

Without an effective prophylactic solution, infections from SARS-CoV-2 continue to rise worldwide with devastating health and economic costs. SARS-CoV-2 gains entry into host cells via an interaction between its Spike protein and the host cell receptor angiotensin converting enzyme 2 (ACE2). Disruption of this interaction confers potent neutralization of viral entry, providing an avenue for vaccine design and for therapeutic antibodies. Here, we develop single-domain antibodies (nanobodies) that potently disrupt the interaction between the SARS-CoV-2 Spike and ACE2. By screening a yeast surface-displayed library of synthetic nanobody sequences, we identified a panel of nanobodies that bind to multiple epitopes on Spike and block ACE2 interaction via two distinct mechanisms. Cryogenic electron microscopy (cryo-EM) revealed that one exceptionally stable nanobody, Nb6, binds Spike in a fully inactive conformation with its receptor binding domains (RBDs) locked into their inaccessible down-state, incapable of binding ACE2. Affinity maturation and structure-guided design of multivalency yielded a trivalent nanobody, mNb6-tri, with femtomolar affinity for SARS-CoV-2 Spike and picomolar neutralization of SARS-CoV-2 infection. mNb6-tri retains stability and function after aerosolization, lyophilization, and heat treatment. These properties may enable aerosol-mediated delivery of this potent neutralizer directly to the airway epithelia, promising to yield a widely deployable, patient-friendly prophylactic and/or early infection therapeutic agent to stem the worst pandemic in a century.

bioRxiv

18218724

10.1088/1748-3182/7/3/036014

Locomotion of Mexican jumping beans.

The Mexican jumping bean, Laspeyresia saltitans, consists of a hollow seed housing a moth larva. Heating by the sun induces movements by the larva which appear as rolls, jumps and flips by the bean. In this combined experimental, numerical and robotic study, we investigate this unique means of rolling locomotion. Time-lapse videography is used to record bean trajectories across a series of terrain types, including one-dimensional channels and planar surfaces of varying inclination. We find that the shell encumbers the larva's locomotion, decreasing its speed on flat surfaces by threefold. We also observe that the two-dimensional search algorithm of the bean resembles the run-and-tumble search of bacteria. We test this search algorithm using both an agent-based simulation and a wheeled Scribbler robot. The algorithm succeeds in propelling the robot away from regions of high temperature and may have application in biomimetic micro-scale navigation systems.

Bioinspiration & Biomimetics

19871615

10.1016/J.JTBI.2017.09.017

Optimal construction of army ant living bridges.

Integrating the costs and benefits of collective behaviors is a fundamental challenge to understanding the evolution of group living. These costs and benefits can rarely be quantified simultaneously due to the complexity of the interactions within the group, or even compared to each other because of the absence of common metrics between them. The construction of 'living bridges' by New World army ants - which they use to shorten their foraging trails - is a unique example of a collective behavior where costs and benefits have been experimentally measured and related to each other. As a result, it is possible to make quantitative predictions about when and how the behavior will be observed. In this paper, we extend a previous mathematical model of these costs and benefits to much broader domain of applicability. Specifically, we exhibit a procedure for analyzing the optimal formation, and final configuration, of army ant living bridges given a means to express the geometrical configuration of foraging path obstructions. Using this procedure, we provide experimentally testable predictions of the final bridge position, as well as the optimal formation process for certain cases, for a wide range of scenarios, which more closely resemble common terrain obstacles that ants encounter in nature. As such, our framework offers a rare benchmark for determining the evolutionary pressures governing the evolution of a naturally occurring collective animal behavior.

Journal of Theoretical Biology

220729957

10.1088/1748-3190/ABA8AC

Aerodynamic performance of flexible flapping wings deformed by slack angle.

Wing flexibility is unavoidable for flapping wing flyers to ensure a lightweight body and for higher payload allowances on board. It also effectively minimizes the inertia force from high-frequency wingbeat motion. However, related studies that attempt to clarify the essence of wing flexibility remain insufficient. Here, a parametric study of a flexible wing was conducted as part of the effort to build an aerodynamic model and analyze its aerodynamic performance. The Quasi-steady (QS) modelling was adopted with experimentally determined translational forces. These forces were determined from 84 flexible wing cases while varying the angle of attack at the wing root and the flexibility parameter, slack angle , with 19 additional rigid wing cases. This study found for optimum lift generation to exceed 45° irrespective of . The coefficient curves were well-fitted with a cubed-sine function. The model was rigorously validated with various wing kinematics, giving a good estimation of the experimental results. The estimated error was less than 5%, 6%, and 8% for the lift, drag, and moment, respectively, considering fast to moderate wing kinematics. The study was extended to analyze the pure aerodynamic performance of the flexible wing. The most suitable wing for a flapping-wing micro-aerial vehicle (FWMAV) wing design with a simple vein structure was found to be the 5° slack-angled wing. The inference from this study further shows that a small amount of deformation is needed to increase the lift, as observed in natural flyers. Thus, wing deformation could allow living flyers to undertake less pitching motion in order to reduce the mechanical power and increase the efficiency of their wings.

Bioinspiration & Biomimetics

224805416

10.1098/RSPB.2020.1748

Bird wings act as a suspension system that rejects gusts

Musculoskeletal systems cope with many environmental perturbations without neurological control. These passive preflex responses aid animals to move swiftly through complex terrain. Whether preflexes play a substantial role in animal flight is uncertain. We investigated how birds cope with gusty environments and found that their wings can act as a suspension system, reducing the effects of vertical gusts by elevating rapidly about the shoulder. This preflex mechanism rejected the gust impulse through inertial effects, diminishing the predicted impulse to the torso and head by 32% over the first 80 ms, before aerodynamic mechanisms took effect. For each wing, the centre of aerodynamic loading aligns with the centre of percussion, consistent with enhancing passive inertial gust rejection. The reduced motion of the torso in demanding conditions simplifies crucial tasks, such as landing, prey capture and visual tracking. Implementing a similar preflex mechanism in future small-scale aircraft will help to mitigate the effects of gusts and turbulence without added computational burden.

Proceedings of The Royal Society B: Biological Sciences

226042328

10.1242/JEB.226654

Remoras pick where they stick on blue whales

ABSTRACT Animal-borne video recordings from blue whales in the open ocean show that remoras preferentially adhere to specific regions on the surface of the whale. Using empirical and computational fluid dynamics analyses, we show that remora attachment was specific to regions of separating flow and wakes caused by surface features on the whale. Adhesion at these locations offers remoras drag reduction of up to 71–84% compared with the freestream. Remoras were observed to move freely along the surface of the whale using skimming and sliding behaviors. Skimming provided drag reduction as high as 50–72% at some locations for some remora sizes, but little to none was available in regions where few to no remoras were observed. Experimental work suggests that the Venturi effect may help remoras stay near the whale while skimming. Understanding the flow environment around a swimming blue whale will inform the placement of biosensor tags to increase attachment time for extended ecological monitoring. Highlighted Article: Analysis of previously undocumented skimming and sliding behaviors used by remoras reveals they preferentially adhere to areas with reduced drag on blue whales.

The Journal of Experimental Biology

225098396

10.1016/J.ANBEHAV.2020.09.014

Quadratic resource value assessment during mantis shrimp (Stomatopoda) contests

Resource value assessment, in which competitors adjust behaviours according to the perceived value of a contested resource, is well described in animal contests. Such assessment is usually assumed to be categorical or linear; for example, males fight more aggressively when females are present than absent, or as female fecundity increases. Here, to our knowledge for the first time, we show quadratic resource value assessment, in which resource value is highest at a certain level and decreases in either direction. The mantis shrimp Neogonodactylus bredini occupies coral rubble burrows in a size-assortative manner: individuals of a certain body size inhabit burrows of a certain size. Using mock burrows of various sizes, we tested whether mantis shrimp (1) chose burrows predicted to be the best fit for their body size and (2) were more aggressive during, endured higher costs during and were more likely to win contests over burrows predicted to be best fit. Individuals chose burrows larger than their predicted best fit burrows. In contests, intruders without burrows were more likely to evict burrow residents when the burrow was slightly smaller than the intruder's predicted best fit size. Intruder success decreased as relative burrow size increased or decreased from this value. Intruders won by delivering more strikes and by being aggressive first. In contrast to intruders, burrow residents showed little evidence of resource value assessment. A literature review revealed that quadratic resource value assessment may play a role in contests over resources from territories to parasite hosts. Therefore, our results impact theoretical models of contest behaviour and may lend insight to how contests affect resource distributions.

Animal Behaviour

7234675

10.1152/PHYSREV.00016.2016

Molecular Physiology of Freeze Tolerance in Vertebrates.

Freeze tolerance is an amazing winter survival strategy used by various amphibians and reptiles living in seasonally cold environments. These animals may spend weeks or months with up to ∼65% of their total body water frozen as extracellular ice and no physiological vital signs, and yet after thawing they return to normal life within a few hours. Two main principles of animal freeze tolerance have received much attention: the production of high concentrations of organic osmolytes (glucose, glycerol, urea among amphibians) that protect the intracellular environment, and the control of ice within the body (the first putative ice-binding protein in a frog was recently identified), but many other strategies of biochemical adaptation also contribute to freezing survival. Discussed herein are recent advances in our understanding of amphibian and reptile freeze tolerance with a focus on cell preservation strategies (chaperones, antioxidants, damage defense mechanisms), membrane transporters for water and cryoprotectants, energy metabolism, gene/protein adaptations, and the regulatory control of freeze-responsive hypometabolism at multiple levels (epigenetic regulation of DNA, microRNA action, cell signaling and transcription factor regulation, cell cycle control, and anti-apoptosis). All are providing a much more complete picture of life in the frozen state.

Physiological Reviews

110250318

10.1007/978-3-211-99749-9_1

Nature as model for technical sensors

Summary form only given. Sensors and sensing are essential for all forms of life. Correspondingly there is a fascinating richness and diversity of sensory systems throughout the animal kingdom. Animals use sensory input not only for communication, but also for the detection, discrimination and localization of animate and inanimate objects. In addition sensory systems provide basic cues for spatial orientation and navigation. Both the structure and the physiology of sensory systems reflect the natural environment in which an animal lives and the needs of the animal. Accordingly, the relevant and often complex stimuli and noise conditions, which natural sensors evolved to cope with, have to be found and applied, to fully understand any sensory system. This is a particular challenge in cases where animals show sensory capabilities alien to human perceptions. This presentation focuses on two sensory systems that humans and most animals do not have: the infrared sensory system of pyrophilous beetles and the electrosensory system of weakly electric fish. I will show that these sensory systems not only have remarkable features but can also be used as a model for the development of novel technical sensors.

IEEE Sensors

219706225

10.1073/PNAS.1918297117

An energy landscape approach to locomotor transitions in complex 3D terrain

Significance Effective locomotion in nature happens by transitioning across multiple modes (e.g., walk, run, climb). Using laboratory experiments on a model system, we demonstrate that an energy landscape approach helps understand how multipathway transitions across locomotor modes in complex 3D terrain statistically emerge from physical interaction. Animals’ and robots’ locomotor modes are attracted to basins of a potential energy landscape. They can use kinetic energy fluctuation from oscillatory self-propulsion to cross potential energy barriers, escaping from one basin and reaching another to make locomotor transitions. Our first-principle energy landscape approach is the beginning of a statistical physics theory of locomotor transitions in complex terrain. It will help understand and predict how animals, and how robots should, move through the real world. Effective locomotion in nature happens by transitioning across multiple modes (e.g., walk, run, climb). Despite this, far more mechanistic understanding of terrestrial locomotion has been on how to generate and stabilize around near–steady-state movement in a single mode. We still know little about how locomotor transitions emerge from physical interaction with complex terrain. Consequently, robots largely rely on geometric maps to avoid obstacles, not traverse them. Recent studies revealed that locomotor transitions in complex three-dimensional (3D) terrain occur probabilistically via multiple pathways. Here, we show that an energy landscape approach elucidates the underlying physical principles. We discovered that locomotor transitions of animals and robots self-propelled through complex 3D terrain correspond to barrier-crossing transitions on a potential energy landscape. Locomotor modes are attracted to landscape basins separated by potential energy barriers. Kinetic energy fluctuation from oscillatory self-propulsion helps the system stochastically escape from one basin and reach another to make transitions. Escape is more likely toward lower barrier direction. These principles are surprisingly similar to those of near-equilibrium, microscopic systems. Analogous to free-energy landscapes for multipathway protein folding transitions, our energy landscape approach from first principles is the beginning of a statistical physics theory of multipathway locomotor transitions in complex terrain. This will not only help understand how the organization of animal behavior emerges from multiscale interactions between their neural and mechanical systems and the physical environment, but also guide robot design, control, and planning over the large, intractable locomotor-terrain parameter space to generate robust locomotor transitions through the real world.

Proceedings of the National Academy of Sciences of the United States of America

213640293

10.1016/B978-0-12-816770-0.00020-4

Biomimicry as a design tool for nanocontainers: The “shape of things to come” in drug delivery

Abstract Nanocontainers embody a “compartmentalized” structural archetype with the potential to operate on a dimensional scale that can either assimilate or be integrated within bio-driven processes. With expected improvements in sensitive diagnostic assays for early disease detection (e.g., CTCs or circulating tumor cells), this has important implications for developing drug delivery technologies to areas of small confinement in the body. Functionalized nanocontainers with tunable surface properties can help stabilize and release therapeutic chemical and biological drugs within nano- and sub-nano spaced cavities. Here, we discuss recent developments in the field of “nanocontainers” that show promise for addressing some of the more challenging aspects of drug therapeutics.

219740641

10.1016/J.XCRP.2020.100060

Inhibiting Freeze-Thaw Damage in Cement Paste and Concrete by Mimicking Nature’s Antifreeze

Summary Since the 1930s, surfactant-based air-entraining admixtures (AEAs) have been used to mitigate freeze-thaw damage in cementitious materials. While effective, entrained air voids weaken concrete and increase its permeability, thereby increasing susceptibility to multiple other forms of in situ degradation. Inspired by nature, we report that a soluble biomimetic antifreeze polymer that displays ice recrystallization inhibition (IRI) and dynamic ice shaping (DIS) activities can prevent damage from ice crystal growth in cement paste and concrete. We first report that polyethylene glycol-graft-polyvinyl alcohol (PEG-PVA) mimics the explicit IRI and DIS activity of native ice-binding proteins in high-pH media characteristic of concrete pore solution. Second, we report that addition of PEG-PVA to cement paste and concrete prevents freeze-thaw damage without entraining air. Taken together, the findings demonstrate an alternative mechanistic approach to AEAs that can be leveraged to prevent damage from ice crystal growth in cementitious materials.

Cell Reports Physical Science

219934809

10.1016/J.MATT.2020.05.011

Structure and Mechanical Adaptability of a Modern Elasmoid Fish Scale from the Common Carp

Summary The carp (Cyprinus carpio) has typical elasmoid scales commonly found on teleosts. They provide protection while retaining flexibility and maneuverability of the fish. The exterior surface of the scale consists of an ultrathin discontinuous mineral layer on top of mineralized woven collagen fibrils. The underlying foundation is composed of two collagenous components. The major one consists of a single-twisted “Bouligand” structure with a twisting angle of 36°. A secondary “sheet-like” structure, formed by thinner collagen fibrils oriented along the thickness direction, acts to increase the integrity of the scale. Here, we identify the deformation and failure mechanisms of the carp scale, revealing slight tensile anisotropy. Using in situ small-angle X-ray scattering during tensile testing, the toughening mechanisms of the scale, including the adaptive structural reorientation of lamellae as well as fibrillar sliding and elastic deformation, are quantified and compared with those of other fish scales.

Matter

226001266

10.1016/J.CUB.2020.09.048

Ogre-Faced, Net-Casting Spiders Use Auditory Cues to Detect Airborne Prey

Prey capture behavior among spiders varies greatly from passive entrapment in webs to running down prey items on foot. Somewhere in the middle are the ogre-faced, net-casting spiders [1] (Deinopidae: Deinopis) that actively capture prey while being suspended within a frame web [2-5]. Using a net held between their front four legs, these spiders lunge downward to ensnare prey from off the ground beneath them. This "forward strike" is sensorially mediated by a massive pair of hypersensitive, night-vision eyes [5-7]. Deinopids can also intercept flying insects with a "backward strike," a ballistically rapid, overhead back-twist, that seems not to rely on visual cues [4, 5, 8]. Past reports have hypothesized a role of acoustic detection in backward strike behavior [4, 5, 8]. Here, we report that the net-casting spider, Deinopis spinosa, can detect auditory stimuli from at least 2 m from the sound source, at or above 60 dB SPL, and that this acoustic sensitivity is sufficient to trigger backward strike behavior. We present neurophysiological recordings in response to acoustic stimulation, both from sound-sensitive areas in the brain and isolated forelegs, which demonstrate a broad range of auditory sensitivity (100-10,000 Hz). Moreover, we conducted behavioral assays of acoustic stimulation that confirm acoustic triggering of backward net-casting by frequencies in harmony with flight tones of known prey. However, acoustic stimulation using higher frequency sounds did not elicit predatory responses in D. spinosa. We hypothesize higher frequencies are emitted by avian predators and that detecting these auditory cues may aid in anti-predator behavior. VIDEO ABSTRACT.

Current Biology

221099148

10.1002/JEZ.B.22988

Evolution of the acoustic startle response of Mexican cavefish.

The ability to detect threatening stimuli and initiate an escape response is essential for survival and under stringent evolutionary pressure. In diverse fish species, acoustic stimuli activate Mauthner neurons, which initiate a C-start escape response. This reflexive behavior is highly conserved across aquatic species and provides a model for investigating the neural mechanism underlying the evolution of escape behavior. Here, we characterize evolved differences in the C-start response between populations of the Mexican cavefish, Astyanax mexicanus. Cave populations of A. mexicanus inhabit an environment devoid of light and macroscopic predators, resulting in evolved differences in various morphological and behavioral traits. We find that the C-start is present in river-dwelling surface fish and multiple populations of cavefish, but that response kinematics and probability differ between populations. The Pachón population of cavefish exhibits an increased response probability, a slower response latency and speed, and reduction of the maximum bend angle, revealing evolved differences between surface and cave populations. Analysis of the responses of two other independently evolved populations of cavefish, revealed the repeated evolution of reduced angular speed. Investigation of surface-cave hybrids reveals a correlation between angular speed and peak angle, suggesting these two kinematic characteristics are related at the genetic or functional levels. Together, these findings provide support for the use of A. mexicanus as a model to investigate the evolution of escape behavior.

Journal of Experimental Zoology

225999071

10.1016/J.CELL.2020.09.008

Molecular Basis of Chemotactile Sensation in Octopus

Animals display wide-ranging evolutionary adaptations based on their ecological niche. Octopuses explore the seafloor with their flexible arms using a specialized "taste by touch" system to locally sense and respond to prey-derived chemicals and movement. How the peripherally distributed octopus nervous system mediates relatively autonomous arm behavior is unknown. Here, we report that octopus arms use a family of cephalopod-specific chemotactile receptors (CRs) to detect poorly soluble natural products, thereby defining a form of contact-dependent, aquatic chemosensation. CRs form discrete ion channel complexes that mediate the detection of diverse stimuli and transduction of specific ionic signals. Furthermore, distinct chemo- and mechanosensory cells exhibit specific receptor expression and electrical activities to support peripheral information coding and complex chemotactile behaviors. These findings demonstrate that the peripherally distributed octopus nervous system is a key site for signal processing and highlight how molecular and anatomical features synergistically evolve to suit an animal's environmental context.

Cell

225080493

10.1038/S43246-020-00078-Y

Nacre toughening due to cooperative plastic deformation of stacks of co-oriented aragonite platelets

Nacre’s structure-property relationships have been a source of inspiration for designing advanced functional materials with both high strength and toughness. These outstanding mechanical properties have been mostly attributed to the interplay between aragonite platelets and organic matrices in the typical brick-and-mortar structure. Here, we show that crystallographically co-oriented stacks of aragonite platelets, in both columnar and sheet nacre, define another hierarchical level that contributes to the toughening of nacre. By correlating piezo-Raman and micro-indentation results, we quantify the residual strain energy associated with strain hardening capacity. Our findings suggest that the aragonite stacks, with characteristic dimensions of around 20 µm, effectively store energy through cooperative plastic deformation. The existence of a larger length scale beyond the brick-and-mortar structure offers an opportunity for a more efficient implementation of biomimetic design. The hierarchical structure of nacre is known to contribute to its high strength and toughness, providing inspiration for many biomimetic materials. Here, co-oriented 20 µm stacks of aragonite platelets are shown to contribute to the toughness of nacre, defining a new characteristic length scale.

Communications Materials

224819498

10.1038/S41598-020-73900-9

A possible link between coral reef success, crustose coralline algae and the evolution of herbivory

Crustose coralline red algae (CCA) play a key role in the consolidation of many modern tropical coral reefs. It is unclear, however, if their function as reef consolidators was equally pronounced in the geological past. Using a comprehensive database on ancient reefs, we show a strong correlation between the presence of CCA and the formation of true coral reefs throughout the last 150 Ma. We investigated if repeated breakdowns in the potential capacity of CCA to spur reef development were associated with sea level, ocean temperature, CO2 concentration, CCA species diversity, and/or the evolution of major herbivore groups. Model results show that the correlation between the occurrence of CCA and the development of true coral reefs increased with CCA diversity and cooler ocean temperatures while the diversification of herbivores had a transient negative effect. The evolution of novel herbivore groups compromised the interaction between CCA and true reef growth at least three times in the investigated time interval. These crises have been overcome by morphological adaptations of CCA.

Scientific Reports

227159764

10.1073/PNAS.2019140117

Natural hybrid silica/protein superstructure at atomic resolution

Significance Using hybrid silica/protein templates, nature has mastered the fabrication of extremely complex macroscopic glass assemblies. Highly symmetric skeletal elements in demosponges are formed following a unique biomineralization mechanism in which polycondensation of an inherently disordered amorphous silica is guided by highly ordered proteinaceous filaments. Here we provide a comprehensive three-dimensional atomistic view of this hybrid assembly. The structure, occurring in the crystalline form in vivo, was measured in situ using the serial crystallography method. Together with a high-resolution transmission electron microscopy and energy-dispersive X-ray spectroscopy study, we provide structural, chemical, and functional information on a naturally forming hybrid mineral/organic crystal. Formation of highly symmetric skeletal elements in demosponges, called spicules, follows a unique biomineralization mechanism in which polycondensation of an inherently disordered amorphous silica is guided by a highly ordered proteinaceous scaffold, the axial filament. The enzymatically active proteins, silicateins, are assembled into a slender hybrid silica/protein crystalline superstructure that directs the morphogenesis of the spicules. Furthermore, silicateins are known to catalyze the formation of a large variety of other technologically relevant organic and inorganic materials. However, despite the biological and biotechnological importance of this macromolecule, its tertiary structure was never determined. Here we report the atomic structure of silicatein and the entire mineral/organic hybrid assembly with a resolution of 2.4 Å. In this work, the serial X-ray crystallography method was successfully adopted to probe the 2-µm-thick filaments in situ, being embedded inside the skeletal elements. In combination with imaging and chemical analysis using high-resolution transmission electron microscopy, we provide detailed information on the enzymatic activity of silicatein, its crystallization, and the emergence of a functional three-dimensional silica/protein superstructure in vivo. Ultimately, we describe a naturally occurring mineral/protein crystalline assembly at atomic resolution.

Proceedings of the National Academy of Sciences of the United States of America

225098817

10.1073/PNAS.2013250117

Time cells in the human hippocampus and entorhinal cortex support episodic memory

Significance Time cells are neurons in the hippocampus and entorhinal cortex that fire at specific moments within a cognitive task or experience. While many prominent theories of memory encoding offer time cells as the source of the temporal component to memory, they have never been observed in human recordings. We identify time cell populations in the medial temporal lobe of humans during memory encoding and retrieval. Further, we demonstrate that the stability of the time signal provided by time cells during encoding influences the ability to temporally order memories at time of retrieval. The organization of temporal information is critical for the encoding and retrieval of episodic memories. In the rodent hippocampus and entorhinal cortex, evidence accumulated over the last decade suggests that populations of “time cells” in the hippocampus encode temporal information. We identify time cells in humans using intracranial microelectrode recordings obtained from 27 human epilepsy patients who performed an episodic memory task. We show that time cell activity predicts the temporal organization of retrieved memory items. We also uncover evidence of ramping cell activity in humans, which represents a complementary type of temporal information. These findings establish a cellular mechanism for the representation of temporal information in the human brain needed to form episodic memories.

Proceedings of the National Academy of Sciences of the United States of America

226840463

10.1126/SCIADV.ABE0440

High-capacity auditory memory for vocal communication in a social songbird

Zebra finches can quickly form long-term auditory memories of up to 50 conspecifics based on their song or distance call. Effective vocal communication often requires the listener to recognize the identity of a vocalizer, and this recognition is dependent on the listener’s ability to form auditory memories. We tested the memory capacity of a social songbird, the zebra finch, for vocalizer identities using conditioning experiments and found that male and female zebra finches can remember a large number of vocalizers (mean, 42) based solely on the individual signatures found in their songs and distance calls. These memories were formed within a few trials, were generalized to previously unheard renditions, and were maintained for up to a month. A fast and high-capacity auditory memory for vocalizer identity has not been demonstrated previously in any nonhuman animals and is an important component of vocal communication in social species.

Science Advances

225225204

10.1039/D0NA00445F

Photonics in nature and bioinspired designs: sustainable approaches for a colourful world

Biological systems possess nanoarchitectures that have evolved for specific purposes and whose ability to modulate the flow of light creates an extraordinary diversity of natural photonic structures. In particular, the striking beauty of the structural colouration observed in nature has inspired technological innovation in many fields. Intense research has been devoted to mimicking the unique vivid colours with newly designed photonic structures presenting stimuli-responsive properties, with remarkable applications in health care, safety and security. This review highlights bioinspired photonic approaches in this context, starting by presenting many appealing examples of structural colours in nature, followed by describing the versatility of fabrication methods and designed coloured structures. A particular focus is given to optical sensing for medical diagnosis, food control and environmental monitoring, which has experienced a significant growth, especially considering the advances in obtaining inexpensive miniaturized systems, more reliability, fast responses, and the use of label-free layouts. Additionally, naturally derived biomaterials and synthetic polymers are versatile and fit many different structural designs that are underlined. Progress in bioinspired photonic polymers and their integration in novel devices is discussed since recent developments have emerged to lift the expectations of smart, flexible, wearable and portable sensors. The discussion is expanded to give emphasis on additional functionalities offered to related biomedical applications and the use of structural colours in new sustainable strategies that could meet the needs of technological development.

Nanoscale Advances

224852560

10.1016/J.ENBUILD.2020.110313

Bio-inspired cooling technologies and the applications in buildings

Abstract In response to the growing demand for indoor environmental quality (IEQ) and energy efficiency, abundant innovative bio-inspired cooling technologies have been proposed and their applications in buildings have been greatly demonstrated in the previous decades to enhance the benefits of building occupants. IEQ is associated with human health and productivity but maintaining good IEQ requires continuous air-conditioning resulting in a high energy consumption, especially space cooling. Bio-inspired cooling technologies focus on the fundamental mechanisms of heat transfer used by animals or plants which are considered as the keys to create a harmony between buildings and the nature, whereby IEQ can be enhanced while achieving energy efficiency. This review provides a comprehensive summary on the current bio-inspired cooling technologies, including the concepts in the research stage and the well-developed products applied in buildings, and discusses some promising designs that have the most potential for future applications. This paper is structured according to building elements, in which technologies regarding HVAC system, building materials, opaque building envelope and transparent building envelope are reviewed. The heat transfer mechanisms behind each technology including conduction, convection, evaporation or phase change and radiation are discussed. Yet successful green buildings involve a smart thermal management system for which a section is dedicated to discussing various approaches in design optimization. In the last section, a case study simulation of implementation of bio-inspired cooling technologies in a house and its energy efficient performance are analyzed. The authors attempt to motivate the future research and development in energy efficient buildings.

Energy and Buildings

49225173

10.1111/J.1365-3032.2008.00627.X

Vibration‐mediated territoriality in the warty birch caterpillar Drepana bilineata

Abstract The warty birch caterpillar Drepana bilineata produces two distinct types of vibrational signals (mandible drumming and anal scraping) during interactions with conspecifics. Vibrational signalling is characterized using standard and high‐speed videography synchronized with laser‐doppler vibrometry, and behavioural experiments test the hypothesis that signalling functions to advertise occupancy of birch (Betula) leaves. Drumming involves raising the head and striking the leaf with the sharp edges of the open mandibles. Anal scraping involves dragging a pair of specialized oar‐shaped setae against the leaf surface. Staged encounters between leaf residents and conspecific intruders result in the resident signalling, with rates increasing as the intruder moves closer. Intruders signal significantly less often than residents. Conflicts are typically resolved within a few minutes, with the resident winning in 61% of the trials, and the intruder winning in 6%. Contests that last more than 30 min are deemed ‘ties’ and comprise the remaining 33% of trials. The results support the hypothesis that vibrational signals function to advertise leaf occupancy. Vibrational communication is believed to be widespread in Drepanoidea caterpillars, but has only been described in two species to date: D. bilineata (present study) and Drepana arcuata. It is proposed that differences in territorial behaviour and signalling between these species are related to their relative investments in silk leaf mats and shelters. The proximate and ultimate bases for the evolution of vibrational communication in caterpillars are discussed.

Physiological Entomology

8734329

10.1073/PNAS.1213331109

Biologically inspired LED lens from cuticular nanostructures of firefly lantern

Cuticular nanostructures found in insects effectively manage light for light polarization, structural color, or optical index matching within an ultrathin natural scale. These nanostructures are mainly dedicated to manage incoming light and recently inspired many imaging and display applications. A bioluminescent organ, such as a firefly lantern, helps to out-couple light from the body in a highly efficient fashion for delivering strong optical signals in sexual communication. However, the cuticular nanostructures, except the light-producing reactions, have not been well investigated for physical principles and engineering biomimetics. Here we report a unique observation of high-transmission nanostructures on a firefly lantern and its biological inspiration for highly efficient LED illumination. Both numerical and experimental results clearly reveal high transmission through the nanostructures inspired from the lantern cuticle. The nanostructures on an LED lens surface were fabricated by using a large-area nanotemplating and reconfigurable nanomolding with heat-induced shear thinning. The biologically inspired LED lens, distinct from a smooth surface lens, substantially increases light transmission over visible ranges, comparable to conventional antireflection coating. This biological inspiration can offer new opportunities for increasing the light extraction efficiency of high-power LED packages.

Proceedings of the National Academy of Sciences of the United States of America

218961994

10.1039/D0FD00034E

Scattering of ultraviolet light by avian eggshells.

Eggshells are essential for the reproduction of birds since the optical properties of shells may have an impact on biological functions such as heating and UV protection, recognition by parents or camouflage. Whereas ultraviolet reflection by some bird eggshells has been recently described, its physical origin remains poorly understood. In this study, we identified a porous structure in eggshells. Using Mie scattering modelling, we found it was most likely responsible for reflectance peaks (intensities of ca. 20-50%) observed in the near-UV range. These peaks were observed by spectrophotometric measurements from eggshells of several breeds of hen, one breed of duck and one breed of quail. This optical response was interpreted in terms of the distinct visual perception of hens and humans: eggshells appearing achromatic for humans proved to be chromatic for hens. Fluorescence emission from these eggs was also characterised and attributed to the presence of protoporphyrin IX and biliverdin IXα in the shells. Electron microscopy observations revealed the presence of pores within the so-called calcified shell part (i.e., at depths between ca. 20 μm and ca. 240 μm from the eggshell's outer surface). Mercury intrusion porosimetry allowed us to quantify the pore size distribution. Simulations of the UV response of this porous structure using Mie scattering theory as well as an effective approach accounting for multiple scattering indicate that these pores are responsible for the backscattering peaks observed in the UV range, in the case of beige hen eggshells. Due to the similarities between the pore size distributions observed for beige hen eggshells and other investigated poultry eggshells, we expect Mie backscattering to be the origin of the UV response of the eggshells of many other bird species.

Faraday Discussions

2482853

10.1663/0006-8101(2007)73[290:ADAMLR]2.0.CO;2

A dehydration avoidance mechanism: Leaf rolling

Plants have several defense mechanisms against unfavorable environmental conditions. One of these mechanisms is leaf rolling. In this review, leaf rolling as a response to water deficit stress and biochemical changes during leaf rolling in higher plants are reported. For instance, the activities of some enzymes and osmotic substances change during leaf rolling. Leaf rolling increases drought resistance in numerous species in theGramineae as well as inCtenanthe setosa, a perennial herbaceous plant that is a suitable model for use in studies of leaf rolling.ZusammenfassungPflanzen besitzen Schutzmechanismen gegen ungünstige Umweltbedingungen. Einer dieser Mechanismen ist das Einrollen der Blätter. In diesem Übersichtsartikel wird erstmals über die Bedeutung des Einrollens der Blätter als Antwort auf Wassermangel und von biochemischen Änderungen während des Einrollens der Blätter bei höheren Pflanzen berichtet. Das Einrollen der Blätter ist nicht nur eine Reaktion der Pflanze auf Wassermangel, es treten auch biochemische Veränderungen zusammen mit dem Einrollen der Blätter auf. Zum Beispiel verändern sich einige Enzymaktivitäten und osmotisch-aktive Stoffe während des Einrollens der Blätter. Das Einrollen der Blätter erhöht die Widerstandsfähigkeit gegen Trockenheit bei vielen Gramineen wieCtenanthe setosa. C. setosa, eine mehrjährige krautige Pflanze, ist eine gute Modellpflanze für Untersuchungen des Einrollens der Blätter.

Botanical Review

226312642

10.1021/ACS.NANOLETT.0C03618

A Pearl Spectrometer.

Information recovery from incomplete measurements, typically performed by a numerical means, is beneficial in a variety of classical and quantum signal processing. Random and sparse sampling with nanophotonic and light scattering approaches has received attention to overcome the hardware limitations of conventional spectrometers and hyperspectral imagers but requires high-precision nanofabrications and bulky media. We report a simple spectral information processing scheme in which light transport through an Anderson-localized medium serves as an entropy source for compressive sampling directly in the frequency domain. As implied by the "lustrous" reflection originating from the exquisite multilayered nanostructures, a pearl (or mother-of-pearl) allows us to exploit the spatial and spectral intensity fluctuations originating from strong light localization for extracting salient spectral information with a compact and thin form factor. Pearl-inspired light localization in low-dimensional structures can offer an alternative of spectral information processing by hybridizing digital and physical properties at a material level.

Nano Letters

229262907

10.1093/IOB/OBAA031

Multiple Degrees of Freedom in the Fish Skull and Their Relation to Hydraulic Transport of Prey in Channel Catfish

Synopsis Fish perform many complex manipulation behaviors without hands or flexible muscular tongues, instead relying on more than 20 movable skeletal elements in their highly kinetic skulls. How fish use their skulls to accomplish these behaviors, however, remains unclear. Most previous mechanical models have represented the fish skull using one or more planar four-bar linkages, which have just a single degree of freedom (DoF). In contrast, truncated-cone hydrodynamic models have assumed up to five DoFs. In this study, we introduce and validate a 3D mechanical linkage model of a fish skull that incorporates the pectoral girdle and mandibular and hyoid arches. We validate this model using an in vivo motion dataset of suction feeding in channel catfish and then use this model to quantify the DoFs in the fish skull, to categorize the motion patterns of the cranial linkage during feeding, and to evaluate the association between these patterns and food motion. We find that the channel catfish skull functions as a 17-link, five-loop parallel mechanism. Despite having 19 potential DoFs, we find that seven DoFs are sufficient to describe most of the motion of the cranial linkage, consistent with the fish skull functioning as a multi-DoF, manipulation system. Channel catfish use this linkage to generate three different motion patterns (rostrocaudal wave, caudorostral wave, and compressive wave), each with its own associated food velocity profile. These results suggest that biomechanical manipulation systems must have a minimum number of DoFs to effectively control objects, whether in water or air.

Integrative Organismal Biology (Oxford, England)

16824428

10.1098/RSIF.2014.1294

Eyelashes divert airflow to protect the eye

Eyelashes are ubiquitous, although their function has long remained a mystery. In this study, we elucidate the aerodynamic benefits of eyelashes. Through anatomical measurements, we find that 22 species of mammals possess eyelashes of a length one-third the eye width. Wind tunnel experiments confirm that this optimal eyelash length reduces both deposition of airborne particles and evaporation of the tear film by a factor of two. Using scaling theory, we find this optimum arises because of the incoming flow's interactions with both the eye and eyelashes. Short eyelashes create a stagnation zone above the ocular surface that thickens the boundary layer, causing shear stress to decrease with increasing eyelash length. Long eyelashes channel flow towards the ocular surface, causing shear stress to increase with increasing eyelash length. These competing effects result in a minimum shear stress for intermediate eyelash lengths. This design may be employed in creating eyelash-inspired protection for optical sensors.

Journal of the Royal Society Interface

225128876

10.1016/J.JOULE.2020.09.013

Eco-Mimicry Opens New Doors for Bioprocess Engineers

The natural world blends microenvironments to create a continuum of spatial niches wherein microbial consortia participate in metabolic exchanges. The capability with which nature selects a consortium to complement a given niche is often taken for granted. Not by Shahab et al. (2020), however, who created a synthetic microbial consortium to mediate a multi-step bioprocess in a single bioreactor system. The concept affords a fair degree of modularity in the choice of biocatalyst and a reasonable level of process control, thus making it an engineering tool.

Joule

53503496

10.1242/JEB.178905

Mammals repel mosquitoes with their tails

ABSTRACT The swinging of a mammal's tail has long been thought to deter biting insects, which, in cows, can drain up to 0.3 liters of blood per day. How effective is a mammal's tail at repelling insects? In this combined experimental and theoretical study, we filmed horses, zebras, elephants, giraffes and dogs swinging their tails. The tail swings at triple the frequency of a gravity-driven pendulum, and requires 27 times more power input. Tails can also be used like a whip to directly strike at insects. This whip-like effect requires substantial torques from the base of the tail on the order of 101–102 N m, comparable to the torque of a sedan, but still within the physical limits of the mammal. Based on our findings, we designed and built a mammal tail simulator to simulate the swinging of the tail. The simulator generates mild breezes of 1 m s–1, comparable to a mosquito's flight speed, and sufficient to deter up to 50% of mosquitoes from landing. This study may help us determine new mosquito-repelling strategies that do not depend on chemicals. Highlighted Article: Mammals swing their tails three times faster than a gravity-driven pendulum. Our experiments with artificial tails show that tail motion generates winds sufficient to repel mosquitoes.

The Journal of Experimental Biology

228087051

10.1371/JOURNAL.PONE.0242668

Honey bees (Apis cerana) use animal feces as a tool to defend colonies against group attack by giant hornets (Vespa soror)

Honey bees (genus Apis) are well known for the impressive suite of nest defenses they have evolved to protect their abundant stockpiles of food and the large colonies they sustain. In Asia, honey bees have evolved under tremendous predatory pressure from social wasps in the genus Vespa, the most formidable of which are the giant hornets that attack colonies in groups, kill adult defenders, and prey on brood. We document for the first time an extraordinary collective defense used by Apis cerana against the giant hornet Vespa soror. In response to attack by V. soror, A. cerana workers foraged for and applied spots of animal feces around their nest entrances. Fecal spotting increased after colonies were exposed either to naturally occurring attacks or to chemicals that scout hornets use to target colonies for mass attack. Spotting continued for days after attacks ceased and occurred in response to V. soror, which frequently landed at and chewed on entrances to breach nests, but not Vespa velutina, a smaller hornet that rarely landed at entrances. Moderate to heavy fecal spotting suppressed attempts by V. soror to penetrate nests by lowering the incidence of multiple-hornet attacks and substantially reducing the likelihood of them approaching and chewing on entrances. We argue that A. cerana forages for animal feces because it has properties that repel this deadly predator from nest entrances, providing the first report of tool use by honey bees and the first evidence that they forage for solids that are not derived from plants. Our study describes a remarkable weapon in the already sophisticated portfolio of defenses that honey bees have evolved in response to the predatory threats they face. It also highlights the strong selective pressure honey bees will encounter if giant hornets, recently detected in western North America, become established.

PLOS ONE

229282759

10.1073/PNAS.2009044117

Structure, self-assembly, and properties of a truncated reflectin variant

Significance The investigation of protein-based materials has provided a better understanding of living systems and has led to the development of ubiquitous modern technologies. Within this context, unique cephalopod proteins called reflectins have exhibited promise for biophotonics and bioelectronics applications, but the exploration of reflectins as materials has been hindered by an incomplete understanding of their structures and properties. Here, we resolve the molecular-level structure of a model reflectin variant, establish a straightforward approach to controlling the assembly of this protein, and describe a correlation between its structural characteristics and light-manipulating properties. Taken together, our findings advance current understanding of reflectin-based materials, provide insight into the color-changing capabilities of cephalopods, and afford new opportunities in biochemistry, cellular biology, bioengineering, and optics. Naturally occurring and recombinant protein-based materials are frequently employed for the study of fundamental biological processes and are often leveraged for applications in areas as diverse as electronics, optics, bioengineering, medicine, and even fashion. Within this context, unique structural proteins known as reflectins have recently attracted substantial attention due to their key roles in the fascinating color-changing capabilities of cephalopods and their technological potential as biophotonic and bioelectronic materials. However, progress toward understanding reflectins has been hindered by their atypical aromatic and charged residue-enriched sequences, extreme sensitivities to subtle changes in environmental conditions, and well-known propensities for aggregation. Herein, we elucidate the structure of a reflectin variant at the molecular level, demonstrate a straightforward mechanical agitation-based methodology for controlling this variant’s hierarchical assembly, and establish a direct correlation between the protein’s structural characteristics and intrinsic optical properties. Altogether, our findings address multiple challenges associated with the development of reflectins as materials, furnish molecular-level insight into the mechanistic underpinnings of cephalopod skin cells’ color-changing functionalities, and may inform new research directions across biochemistry, cellular biology, bioengineering, and optics.

Proceedings of the National Academy of Sciences of the United States of America

227914921

10.1098/RSPB.2020.1517

Limb work and joint work minimization reveal an energetic benefit to the elbows-back, knees-forward limb design in parasagittal quadrupeds

Quadrupedal animal locomotion is energetically costly. We explore two forms of mechanical work that may be relevant in imposing these physiological demands. Limb work, due to the forces and velocities between the stance foot and the centre of mass, could theoretically be zero given vertical limb forces and horizontal centre of mass path. To prevent pitching, skewed vertical force profiles would then be required, with forelimb forces high in late stance and hindlimb forces high in early stance. By contrast, joint work—the positive mechanical work performed by the limb joints—would be reduced with forces directed through the hip or shoulder joints. Measured quadruped kinetics show features consistent with compromised reduction of both forms of work, suggesting some degree of, but not perfect, inter-joint energy transfer. The elbows-back, knees-forward design reduces the joint work demand of a low limb-work, skewed, vertical force profile. This geometry allows periods of high force to be supported when the distal segment is near vertical, imposing low moments about the elbow or knee, while the shoulder or hip avoids high joint power despite high moments because the proximal segment barely rotates—translation over this period is due to rotation of the distal segment.

Proceedings of The Royal Society B: Biological Sciences

230508602

10.1038/S41567-020-01069-Z

Dynamics of topological defects and structural synchronization in a forming periodic tissue

Living organisms form a large variety of hierarchically structured extracellular functional tissues. Remarkably, these materials exhibit regularity and structural coherence across multiple length scales, far beyond the size of a single cell. Here, synchrotron-based nanotomographic imaging in combination with machine-learning-based segmentation is used to reveal the structural synchronization process of nacre forming in the shell of the mollusc Unio pictorum . We show that the emergence of this highly regular layered structure is driven by a disorder-to-order transition achieved through the motion and interaction of screw-like structural dislocations with an opposite topological sign. Using an analogy to similar processes observed in liquid-crystalline systems, we demonstrate that these microstructural faults act as dissipative topological defects coupled by an elastic distortion field surrounding their cores. Their mutual annihilation results in structural synchronization that is simulated using the classical Kuramoto model. The developed experimental, theoretical and numerical framework provides a comprehensive physical view of the formation of biogenic materials. Molluscs assemble layers of material in the shells around them with a high level of control. Here the authors observe the structural evolution of layer formation and propose a mechanism reminiscent of topological defect dynamics in liquid crystals.

Nature Physics