Chapter 4 - Insect Cuticular Surface Modifications: Scales and Other Structural Formations
Introduction
The biology of an arthropod is defined by and depends on the cuticle, the non-living exoskeleton that is secreted by the single layer of epidermal cells that constitutes the living part of the body wall. Indeed, the cuticle may be thought of as a sort of “body stocking” which lines all topologically external surfaces of the animal: on a global scale, it projects out to cover all protuberances—wings, limbs, mouthparts, and others—and it pushes in to line the tracheal system, gut, gland ducts, and the like. On a cellular level, a single epidermal cell can push out an extension to make a scale, bristle, hair, papilla, or any of an array of other cuticular structures, or it can draw in to form a chordotonal organ, which may serve as a mechanical or acoustical receptor or participate, perhaps indirectly, in infrared reception (Schmitz et al., 2001). Or the cell can draw in to form a tracheole, one of the capillaries of the tracheal system.
To accomplish all this, cuticle is and must be an adaptable and versatile building material. Andersen (2009a) reviews briefly cuticle as a material, and its roles in the forms and functions of the exoskeleton (Andersen, 2009b, see also Chapter 3). It is light, tough, and strong and can be made rigid, flexible, elastic, rubbery, solid or porous, isotropic or anisotropic, as the needs require. In bulk form, it provides protection and support and can also be the source of various forms of coloration. But it can also be sculpted into fine surface structures that serve a variety of functions. The multiplicity of these is bewildering, but fortunately for our understanding, most of them seem to be variations on a few common themes. Understanding a subset of these will allow us to understand the general principles of such structures, what is known of their development and, perhaps more important, indicate questions, perspectives, and directions for future research. For this reason, rather than attempt an encyclopedic overview of all their forms, the author has chosen to concentrate on those she knows best, the bristles and scales that adorn so many arthropod integuments. We will also consider the cuticular patterns of a couple of relatively new entries, a Collembolan and a member of the Class Pauropoda.
To start, we remind the reader that arthropod “cuticle” is an entire class of materials that can all be tailored as described earlier with respect to their material properties. A main focus here will be the development of this cuticle into the precise and complex patterns that characterize integumental outgrowths. In connection with this development, one might ask how much information is needed to specify a scale, especially one that is specialized, for example, for producing a structural colour. We suspect that it is less than one might imagine, at least in the genome. Where else could the information be harboured and controlled? Emergent properties of the chemical and/or physical processes that are set in motion as development proceeds must contribute in large part to the final pattern formation. In particular, it is becoming clear that two major players in this cellular development are (1) the cytoskeleton, in particular actin filaments and bundles, and (2) the smooth endoplasmic reticulum (SER). We also believe that relatively simple chemical and physical processes (e.g. elastic buckling) participate in the moulding process. And at all times there must be a conversation between the cell, its local environment, and the systems that must interpret and express in cuticle the resulting consensus.
Where possible, the author is going to rely on review articles in order to save on what would otherwise be an astronomical number of references and detailed points. Two excellent and extensive references in the general field of insect cuticle are Neville, 1975, Neville, 1993; two others that focus on structural colours but include much basic information on the underlying cuticular structures are Kinoshita & Yoshioka, 2005, Kinoshita, 2008. Ghiradella (1998) presents an overview of scales and bristles (although some of the interpretations are old) and, in a review of integumental outgrowths of arthropods specialized for walking on water, Bush et al. (2008) present special analyses of the pertinent structures; these authors also review engineering concepts concerning design for cuticular interaction with fluids and fluid interfaces. (There are also numerous reviews in the burgeoning field of insect colour production—see Chapter 5.)
Section snippets
General classes of cuticular outgrowths
Figure 1 presents an overview of just a few of the many possible structures that ornament cuticle; we start with a short review of each.
Wings and scales
Figure 2 presents a fragment of butterfly wing, together with its covering of scales. As is typical in most (but not all) cases there seem to be at least two layers, larger cover scales and smaller ground scales, the latter only partly visible under the former. In fact, the scale bases are arranged in single rows, alternating CGCGCG; double layer appearance is because the smaller scales are tucked under their larger neighbours.
Scales can occur anywhere on an insect body, but most studies have
Introduction to scale structure
Figure 3 presents a diagrammatic view of a fragment of a more or less unspecialized scale (compare Fig. 5, Fig. 6), together with some of the more common variants on this form. The scale starts development as a cylindrical bristle but then flattens so that the final form of its cuticle is typically that of a flat envelope with what we will call an “upper” surface (visible to the outer world) and a “lower” surface (facing the wing). The lower surface is usually featureless, but the upper is
Basic scale patterning
Having now an idea of basic scale structure and of a few of its possible modifications, let us look at actual examples of some of the forms described in Fig. 3. Figure 5 presents a surface view of part of an essentially unspecialized scale. The ridges are topped with slanting lamellae (⁎), which pattern seems to be the more common case. Whatever the slant of the lamellae, the microribs usually run orthogonally down the ridges from them and some of these run across the crossribs to mount the
Overview of macrochaete development
Having surveyed some of the many forms these scales (and bristles) may take, let us look at their development, again with special attention to that in scales. We remind the reader that a more complete discussion of the early stages is found in Ghiradella (1998). We will revisit here the question of development, but in a different context. Ghiradella and Butler (2009) review some of the following material.
The process of macrochaete building begins when an epidermal cell gets a signal to
Two other arthropods
Figure 32 presents a view of Pauropus sp. As a Pauropod, it is a minute relative of the Diplopoda (the class that includes the millipedes). Because of its small size and the fractional Reynolds number3
Discussion
Having now a general idea of the pattern-forming capabilities of the insect epidermal cell, let us step back and take a longer view to see what basic themes may emerge. In his fine review article, Locke (1998) remarks that “Insects are epidermal organisms. They are the prime example of how an infinite complexity of form may be attained by the manipulation of a layer that is only one cell thick.” As various authors have remarked over the years, it is probably this two-dimensionality of body wall
Final thoughts
In closing, let us make several points. As she thinks about these systems, the author comes increasingly to regard the eukaryotic cell as the “real” organism and us multicellular creatures as diverse expressions of its creative drive. Stated another way, the general lability of the developmental processes leading to these patterns and their commonality among the taxa (a theme well expressed by Shubin et al., 2009) suggests that they are unreliable as taxonomic markers. A slight change in timing
Acknowledgments
Over the years, the author is indebted to many who helped, either directly or indirectly in fostering this research. First and foremost, Thomas (and Maria) Eisner first introduced the subject and have supported me in it ever since. Robert Day Allen provided the place to work and learn. William Radigan and Harry L. Frisch were brilliant and able collaborators, and Bob Greenler provided insights into the field of optics. Orley Taylor and David Wright provided specimens and helpful advice. Sam
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The evolution of structural colour in butterflies
2021, Current Opinion in Genetics and DevelopmentCitation Excerpt :Ridge reflectors have evolved independently in multiple lineages and in some cases several times within a lineage, for example, in Heliconius, driven by convergent evolution for mimicry [28•]. Ridge reflectors form during wing scale development, with alternating air and chitin layers attaining optically precise spacing through drying post-eclosion [19]. Electron micrographs by Ghiradella [23] led her to propose that ridge multilayers form by elastic buckling of the cuticle in response to intracellular stresses.
Butterfly inspired functional materials
2021, Materials Science and Engineering R: ReportsCitation Excerpt :This structural type of scale frequently appears in many Morpho butterflies (Figs. 2b, 3 a) [76,78]. Morpho butterfly is famous for its brilliant blue or white color, whose brightness relates to the number of layers and the gap between ridges [5,76]. The more lamellae may lead to high brightness like Morpho rhetenor, while the less layer and larger gap may result in darker color such as Morpho didius (Fig. 3b, c) [70].
Polymorphism of Colias croceus from the Azores caused by differential pterin expression in the wing scales
2020, Journal of Insect PhysiologyHow many scales on the wings? A case study based on Colias crocea (Geoffroy, 1785) (Hexapoda: Lepidoptera, Pieridae)
2020, Arthropod Structure and DevelopmentCitation Excerpt :A scale is basically a flattened sac of cuticle. The upper surface exhibits an intricate system of longitudinal and cross ridges of complex ultrastructure (Ghiradella, 1998, 2010; Dinwiddie et al., 2014). The morphology, diversity and phylogenetic implications in the Lepidoptera deserved early attention (Kellogg, 1894) and have been active fields of research (Downey and Allyn, 1975; Grodnitsky and Kozlov, 1989; Simonsen, 2001).