Chapter 4 - Insect Cuticular Surface Modifications: Scales and Other Structural Formations

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Abstract

The arthropod integument is noted for its surface outgrowths, especially the microchaetes (hairs) and macrochaetes (bristles and scales). These start as hollow projections templated on cellular microvilli or on filopodia (microchaetes), or on larger projections from their parent epidermal cells (macrochaetes).

Ultrastructurally, finished microchaetes are relatively simple, but macrochaetes are typically highly ornamented, some so much so that their surface architecture can produce structural colours. Similarly, macrochaete interiors may be filled with lattices or laminae that may also produce structural colours.

Many of the patterns appear to be variations on relatively few themes, and control of this pattern formation by the epidermal cell appears to reside in particular with two cellular systems, the actin cytoskeleton and the smooth endoplasmic reticulum. This suggests that focused study of these two systems may yield real insight into pattern formation in general, especially in the arthropods and in other armoured organisms.

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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