skip to main content

This content will become publicly available on December 7, 2022

Title: In vivo visualization of butterfly scale cell morphogenesis in Vanessa cardui
During metamorphosis, the wings of a butterfly sprout hundreds of thousands of scales with intricate microstructures and nano-structures that determine the wings’ optical appearance, wetting characteristics, thermodynamic properties, and aerodynamic behavior. Although the functional characteristics of scales are well known and prove desirable in various applications, the dynamic processes and temporal coordination required to sculpt the scales’ many structural features remain poorly understood. Current knowledge of scale growth is primarily gained from ex vivo studies of fixed scale cells at discrete time points; to fully understand scale formation, it is critical to characterize the time-dependent morphological changes throughout their development. Here, we report the continuous, in vivo, label-free imaging of growing scale cells of Vanessa cardui using speckle-correlation reflection phase microscopy. By capturing time-resolved volumetric tissue data together with nanoscale surface height information, we establish a morphological timeline of wing scale formation and gain quantitative insights into the underlying processes involved in scale cell patterning and growth. We identify early differences in the patterning of cover and ground scales on the young wing and quantify geometrical parameters of growing scale features, which suggest that surface growth is critical to structure formation. Our quantitative, time-resolved in vivo imaging of butterfly scale more » development provides the foundation for decoding the processes and biomechanical principles involved in the formation of functional structures in biological materials. « less
; ; ; ;
Award ID(s):
Publication Date:
Journal Name:
Proceedings of the National Academy of Sciences
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Heliconius butterflies have bright patterns on their wings that tell potential predators that they are toxic. As a result, predators learn to avoid eating them. Over time, unrelated species of butterflies have evolved similar patterns to avoid predation through a process known as Müllerian mimicry. Worldwide, there are over 180,000 species of butterflies and moths, most of which have different wing patterns. How do genes create this pattern diversity? And do butterflies use similar genes to create similar wing patterns? One of the genes involved in creating wing patterns is called cortex . This gene has a large region of DNA around it that does not code for proteins, but instead, controls whether cortex is on or off in different parts of the wing. Changes in this non-coding region can act like switches, turning regions of the wing into different colours and creating complex patterns, but it is unclear how these switches have evolved. Butterfly wings get their colour from tiny structures called scales, which each have their own unique set of pigments. In Heliconius butterflies, there are three types of scales: yellow/white scales, black scales, and red/orange/brown scales. Livraghi et al. used a DNA editing technique called CRISPR tomore »find out whether the cortex gene affects scale type. First, Livraghi et al. confirmed that deleting cortex turned black and red scales yellow. Next, they used the same technique to manipulate the non-coding DNA around the cortex gene to see the effect on the wing pattern. This manipulation turned a black-winged butterfly into a butterfly with a yellow wing band, a pattern that occurs naturally in Heliconius butterflies. The next step was to find the mutation responsible for the appearance of yellow wing bands in nature. It turns out that a bit of extra genetic code, derived from so-called ‘jumping genes’, had inserted itself into the non-coding DNA around the cortex gene, ‘flipping’ the switch and leading to the appearance of the yellow scales. Genetic information contains the instructions to generate shape and form in most organisms. These instructions evolve over millions of years, creating everything from bacteria to blue whales. Butterfly wings are visual evidence of evolution, but the way their genes create new patterns isn't specific to butterflies. Understanding wing patterns can help researchers to learn how genetic switches control diversity across other species too.« less
  2. Müllerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. Here, we first quantify wing colour pattern differences in the forewing region of 14 co-mimetic colour pattern morphs of the butterfly species Heliconius erato and Heliconius melpomene and measure the extent to which mimicking colour pattern morphs are not perfectly identical. Next, using gene-editing CRISPR/Cas9 KO experiments of the gene WntA , which has been mapped to colour pattern diversity in these butterflies, we explore the exact areas of the wings in which WntA affects colour pattern formation differently in H. erato and H. melpomene. We find that, while the relative size of the forewing pattern is generally nearly identical between co-mimics, the CRISPR/Cas9 KO results highlight divergent boundaries in the wing that prevent the co-mimics from achieving perfect mimicry. We suggest that this mismatch may be explained by divergence in the gene regulatory network that defines wing colour patterning in both species, thus constraining morphological evolution even between closely related species.
  3. Context. Inferences about dark matter, dark energy, and the missing baryons all depend on the accuracy of our model of large-scale structure evolution. In particular, with cosmological simulations in our model of the Universe, we trace the growth of structure, and visualize the build-up of bigger structures from smaller ones and of gaseous filaments connecting galaxy clusters. Aims. Here we aim to reveal the complexity of the large-scale structure assembly process in great detail and on scales from tens of kiloparsecs up to more than 10 Mpc with new sensitive large-scale observations from the latest generation of instruments. We also aim to compare our findings with expectations from our cosmological model. Methods. We used dedicated SRG/eROSITA performance verification (PV) X-ray, ASKAP/EMU Early Science radio, and DECam optical observations of a ~15 deg 2 region around the nearby interacting galaxy cluster system A3391/95 to study the warm-hot gas in cluster outskirts and filaments, the surrounding large-scale structure and its formation process, the morphological complexity in the inner parts of the clusters, and the (re-)acceleration of plasma. We also used complementary Sunyaev-Zeldovich (SZ) effect data from the Planck survey and custom-made Galactic total (neutral plus molecular) hydrogen column density maps based onmore »the HI4PI and IRAS surveys. We relate the observations to expectations from cosmological hydrodynamic simulations from the Magneticum suite. Results. We trace the irregular morphology of warm and hot gas of the main clusters from their centers out to well beyond their characteristic radii, r 200 . Between the two main cluster systems, we observe an emission bridge on large scale and with good spatial resolution. This bridge includes a known galaxy group but this can only partially explain the emission. Most gas in the bridge appears hot, but thanks to eROSITA’s unique soft response and large field of view, we discover some tantalizing hints for warm, truly primordial filamentary gas connecting the clusters. Several matter clumps physically surrounding the system are detected. For the “Northern Clump,” we provide evidence that it is falling towards A3391 from the X-ray hot gas morphology and radio lobe structure of its central AGN. Moreover, the shapes of these X-ray and radio structures appear to be formed by gas well beyond the virial radius, r 100 , of A3391, thereby providing an indirect way of probing the gas in this elusive environment. Many of the extended sources in the field detected by eROSITA are also known clusters or new clusters in the background, including a known SZ cluster at redshift z = 1. We find roughly an order of magnitude more cluster candidates than the SPT and ACT surveys together in the same area. We discover an emission filament north of the virial radius of A3391 connecting to the Northern Clump. Furthermore, the absorption-corrected eROSITA surface brightness map shows that this emission filament extends south of A3395 and beyond an extended X-ray-emitting object (the “Little Southern Clump”) towards another galaxy cluster, all at the same redshift. The total projected length of this continuous warm-hot emission filament is 15 Mpc, running almost 4 degrees across the entire eROSITA PV observation field. The Northern and Southern Filament are each detected at >4 σ . The Planck SZ map additionally appears to support the presence of both new filaments. Furthermore, the DECam galaxy density map shows galaxy overdensities in the same regions. Overall, the new datasets provide impressive confirmation of the theoretically expected structure formation processes on the individual system level, including the surrounding warm-hot intergalactic medium distribution; the similarities of features found in a similar system in the Magneticum simulation are striking. Our spatially resolved findings show that baryons indeed reside in large-scale warm-hot gas filaments with a clumpy structure.« less
  4. Modification of serially homologous structures is a common avenue towards functional innovation in developmental evolution, yet ancestral affinities among serial homologues may be obscured as structure-specific modifications accumulate over time. We sought to assess the degree of homology to wings of three types of body wall projections commonly observed in scarab beetles: (i) the dorsomedial support structures found on the second and third thoracic segments of pupae, (ii) the abdominal support structures found bilaterally in most abdominal segments of pupae, and (iii) the prothoracic horns which depending on species and sex may be restricted to pupae or also found in adults. We functionally investigated 14 genes within, as well as two genes outside, the canonical wing gene regulatory network to compare and contrast their role in the formation of each of the three presumed wing serial homologues. We found 11 of 14 wing genes to be functionally required for the proper formation of lateral and dorsal support structures, respectively, and nine for the formation of prothoracic horns. At the same time, we document multiple instances of divergence in gene function across our focal structures. Collectively, our results support the hypothesis that dorsal and lateral support structures as well as prothoracicmore »horns share a developmental origin with insect wings. Our findings suggest that the morphological and underlying gene regulatory diversification of wing serial homologues across species, life stages and segments has contributed significantly to the extraordinary diversity of arthropod appendages and outgrowths.« less
  5. Abstract

    The wings of Lepidoptera contain a matrix of living cells whose function requires appropriate temperatures. However, given their small thermal capacity, wings can overheat rapidly in the sun. Here we analyze butterfly wings across a wide range of simulated environmental conditions, and find that regions containing living cells are maintained at cooler temperatures. Diverse scale nanostructures and non-uniform cuticle thicknesses create a heterogeneous distribution of radiative cooling that selectively reduces the temperature of structures such as wing veins and androconial organs. These tissues are supplied by circulatory, neural and tracheal systems throughout the adult lifetime, indicating that the insect wing is a dynamic, living structure. Behavioral assays show that butterflies use wings to sense visible and infrared radiation, responding with specialized behaviors to prevent overheating of their wings. Our work highlights the physiological importance of wing temperature and how it is exquisitely regulated by structural and behavioral adaptations.