Annie Jessop

Nature offers a remarkable diversity of nanomaterials that have extraordinary functional and structural properties. Intrinsic to nature is the impressive ability to form complex ordered nanomaterials via self-organization. One particularly intriguing nanostructure is the gyroid, a network-like structure exhibiting high symmetry and complex topology. Although its existence in cells and tissues across many biological kingdoms is well documented, how and why it forms remains elusive and uncovering these formation mechanisms will undoubtedly inform bioinspired designs. A beautiful example is the smooth single gyroid that is found in the wing scales of several butterflies, where it behaves as a photonic crystal generating a vibrant green color. Here, we report that the gyroid structures of the Emerald-patched Cattleheart, Parides sesostris, develop as woven fibrillar structures, in contrast to the commonly held assumption that they form as smooth constructs. Ultramicroscopy of pupal tissue reveals that the gyroid geometry consists of helical weavings of fibers, akin to hyperbolic line patterns decorating the gyroid. Interestingly, despite their fibrillar nature, electron diffraction reveals the absence of crystalline order within this material. Similar fibrillar structures are also observed in the mature wing scales of P. sesostris specimens with surgically altered pupal development, leading to a blue coloration. Our findings not only introduce a variation of the gyroid in biology but also have significant implications for our understanding of its formation in nature.

Visual ecology, the study of how animals acquire and respond to visual information in nature, has grown rapidly over the past few decades. Research in this field has transformed our understanding of fundamental processes, such as the neurobiological basis of behavior and the diversification of species through sensory drive. The recent growth in the field has been accompanied by leaps in our understanding of the diversity of visual systems and in the development of novel technologies and techniques (for example, those allowing us to measure scenes and signals). With such growth, however, it is more important than ever to integrate wide perspectives and expertise to move the field forward in the most productive way. To that end, in summer 2024, 30 visual ecologists from around the world - spanning all career stages - met to discuss the state of the field. From that meeting, we identified two broad emerging themes in the study of visual ecology. (1) Can we further 'step inside' the perceptual experience of a non-human animal? (2) Can foundational 'rules' of vision and visual stimuli be identified? Although large questions such as these can feel unanswerable, this is where some of the most exciting discoveries in visual ecology remain to be made. Here, we outline eight relevant areas of research and identify ways in which researchers can bring us closer to answering these complex questions.

The ocean's midwater is a uniquely challenging yet predictable and simple visual environment. The need to see without being seen in this dim, open habitat has led to extraordinary visual adaptations. To understand these adaptations, we compared the morphological and functional differences between the eyes of three hyperiid amphipods—Hyperia galba, Streetsia challengeri and Phronima sedentaria. Combining micro-CT data with computational modelling, we mapped visual field topography and predicted detection distances for visual targets viewed in different directions through mesopelagic depths. Hyperia's eyes provide a wide visual field optimized for spatial vision over short distances, while Phronima's and Streetsia's eyes have the potential to achieve greater sensitivity and longer detection distances using spatial summation. These improvements come at the cost of smaller visual fields, but this loss is compensated for by a second pair of eyes in Phronima and by behaviour in Streetsia. The need to improve sensitivity while minimizing visible eye size to maintain crypsis has likely driven the evolution of hyperiid eye diversity. Our results provide an integrative look at how these elusive animals have adapted to the unique visual challenges of the mesopelagic.

Biophotonic nanostructures in butterfly wing scales remain fascinating examples of biological functional materials, with intriguing open questions with regard to formation and evolutionary function. One particularly interesting butterfly species, Erora opisena (Lycaenidae: Theclinae), develops wing scales that contain three-dimensional photonic crystals that closely resemble a single gyroid geometry. Unlike most other gyroid-forming butterflies, E. opisena develops discrete gyroid crystallites with a pronounced size gradient hinting at a developmental sequence frozen in time. Here, we present a novel application of a hyperspectral (wavelength-resolved) microscopy technique to investigate the ultrastructural organization of these gyroid crystallites in dry, adult wing scales. We show that reflectance corresponds to crystallite size, where larger crystallites reflect green wavelengths more intensely; this relationship could be used to infer size from the optical signal. We further successfully resolve the red-shifted reflectance signal from wing scales immersed in refractive index liquids with varying refractive index, including values similar to water or cytosol. Such photonic crystals with lower refractive index contrast may be similar to the hypothesized nanostructural forms in the developing butterfly scales. The ability to resolve these fainter signals hints at the potential of this facile light microscopy method for in vivo analysis of nanostructure formation in developing butterflies.

The sponge-like biomineralized calcite materials found in echinoderm skeletons are of interest in terms of both structure formation and biological function. Despite their crystalline atomic structure, they exhibit curved interfaces that have been related to known triply periodic minimal surfaces. Here, we investigate the endoskeleton of the sea urchin that has long been known to form a microstructure related to the Primitive surface. Using X-ray tomography, we find that the endoskeleton is organized as a composite material consisting of domains of bicontinuous microstructures with different structural properties. We describe, for the first time, the co-occurrence of ordered single Primitive and single Diamond structures and of a disordered structure within a single skeletal plate. We show that these structures can be distinguished by structural properties including solid volume fraction, trabeculae width and, to a lesser extent, interface area and mean curvature. In doing so, we present a robust method that extracts interface areas and curvature integrals from voxelized datasets using the Steiner polynomial for parallel body volumes. We discuss these very large-scale bicontinuous structures in the context of their function, formation and evolution.

Shadows that are produced across the surface of an object (self-shadows) are potentially an important source of information for visual systems. Animal patterns may exploit this principle for camouflage, using pictorial cues to produce false depth information that manipulates the viewer’s detection/recognition processes. However, pictorial cues could also facilitate camouflage by matching the contrast (e.g. due to shadows) of 3D backgrounds. Aside from studies of countershading (patterning that may conceal depth information), the role of self-shadows in camouflage patterns remains unclear. Here we investigated whether pictorial cues (self-shadows) increase the survival probability of moth-like prey presented to free-living wild bird predators relative to targets without these cues. We manipulated the presence of self-shadows by adjusting the illumination conditions to produce patterned targets under directional lighting (lit from above or from below; self-shadows present) or diffuse lighting (no self-shadows). We used non-patterned targets (uniform colour) as controls. We manipulated the direction of illumination because it has been linked with depth perception in birds; objects lit from above may appear convex while those lit from below can appear concave. As shadows influence contrast, which also determines detectability, we photographed the targets in situ over the observation period, allowing us to evaluate the effect of visual metrics on survival. We found some evidence that patterned targets without self-shadows had a lower probability of survival than patterned targets with self-shadows and targets with uniform colour. Surprisingly, none of the visual metrics explained variation in survival probability. However, predators increased their foraging efficiency over time, suggesting that predator learning may have overridden the benefits afforded by camouflaging coloration.

Nature provides a rich source of information for the design of novel materials; yet there remain significant challenges in the design and manufacture of materials that replicate the form, function, and sustainability of biological solutions. Here, we identify key challenges and promising approaches to the development of materials informed by biology. These challenges fall into two main areas; the first relates to harnessing biological information for materials innovation, including key differences between biological and synthetic materials, and the relationship between structure and function. We propose an approach to materials innovation that capitalizes on biodiversity, together with high-throughput characterization of biological material architectures and properties, linked to environmental and ecological context. The second area relates to the design and manufacture of bioinformed materials, including the physical scale of material architectures and manufacturing scale up. We suggest ways to address these challenges and promising prospects for a bioinformed approach to materials innovation.

Vision in the midwater of the open ocean requires animals to perform visual tasks quite unlike those of any other environment. These tasks consist of detecting small, low contrast objects and point sources against a relatively dim and uniform background. Deep-sea animals have evolved many extraordinary visual adaptations to perform these tasks. Linking eye anatomy to specific selective pressures, however, is challenging, not least because of the many difficulties of studying deep-sea animals. Computational modelling of vision, based on detailed morphological reconstructions of animal eyes, along with underwater optics, offers a chance to understand the specific visual capabilities of individual visual systems. Prior to the work presented here, comprehensive models for apposition compound eyes in the mesopelagic, the dominant eye form of crustaceans, were lacking. We adapted a model developed for single-lens eyes and used it to examine how different parameters affect the model’s ability to detect point sources and extended objects. This new model also allowed us to examine spatial summation as a means to improve visual performance. Our results identify a trade-off between increased depth range over which eyes function effectively and increased distance at which extended objects can be detected. This trade-off is driven by the size of the ommatidial acceptance angle. We also show that if neighbouring ommatidia have overlapping receptive fields, spatial summation helps with all detection tasks, including the detection of bioluminescent point sources. By applying our model to the apposition compound eyes of Phronima, a mesopelagic hyperiid amphipod, we show that the specialisations of the large medial eyes of Phronima improve both the detection of point sources and of extended objects. The medial eyes outperformed the lateral eyes at every modelled detection task. We suggest that the small visual field size of Phronima’s medial eyes and the strong asymmetry between the medial and lateral eyes reflect Phronima’s need for effective vision across a large depth range and its habit of living inside a barrel. The barrel’s narrow aperture limits the usefulness of a large visual field and has allowed a strong asymmetry between the medial and lateral eyes. The model provides a useful tool for future investigations into the visual abilities of apposition compound eyes in the deep sea.

Holopelagic animals were long assumed to have widespread geographic distributions due to the failure to recognize hydrographic species' barriers in the open ocean. As molecular genetic tools are more commonly used to study the ocean's inhabitants, diversity is found to be substantially higher than when inferred from morphological taxonomies alone. Here, we investigate the morphological and genetic diversity of hyperiid amphipods within the genus Paraphronima, currently comprising two supposedly cosmopolitan species. By combining phylogenetic analyses and four species delimitation methods (GMYC, mPTP, bPTP, ABGD), we reveal substantial species-level genetic variation. Instead of two species inhabiting multiple ocean basins, the biogeography of Paraphronima species appears to be limited to more regional scales. Moreover, there is morphological evidence to corroborate the observed genetic diversity. By using an integrative morpho-molecular approach, a third species from the Gulf of California, Paraphronima robisoni sp. nov., is described. Interestingly, the morphological characters that best distinguish the species within the genus are characters of the compound eyes, which have rarely been used for taxonomy despite being the most obvious and varied features of hyperiids. Our results warrant further investigation of presumably cosmopolitan holopelagic amphipods, while we recommend the inclusion of eye morphology in future taxonomic studies.

Colour signals, and the ability to detect them, are important for many animals and can be vital to their survival and fitness. Fiddler crabs use colour information to detect and recognise conspecifics, but their colour vision capabilities remain unclear. Many studies have attempted to measure their spectral sensitivity and identify contributing retinular cells, but the existing evidence is inconclusive. We used electroretinogram (ERG) measurements and intracellular recordings from retinular cells to estimate the spectral sensitivity of Gelasimus dampieri and to track diurnal changes in spectral sensitivity. G. dampieri has a broad spectral sensitivity and is most sensitive to wavelengths between 420 and 460 nm. Selective adaptation experiments uncovered an ultraviolet (UV) retinular cell with a peak sensitivity shorter than 360 nm. The species’ spectral sensitivity above 400 nm is too broad to be fitted by a single visual pigment and using optical modelling, we provide evidence that at least two medium-wavelength sensitive (MWS) visual pigments are contained within a second blue-green sensitive retinular cell. We also found a ∼25 nm diurnal shift in spectral sensitivity towards longer wavelengths in the evening in both ERG and intracellular recordings. Whether the shift is caused by screening pigment migration or changes in opsin expression remains unclear, but the observation shows the diel dynamism of colour vision in this species. Together, these findings support the notion that G. dampieri possesses the minimum requirement for colour vision, with UV and blue/green receptors, and help to explain some of the inconsistent results of previous research.