There has been little research into the evolution of butterfly photonic structures. However, recently two studies were published which had conflicting outcomes. The reason for this lay with different assumptions about the relative contributions of genetic material to the expression, and therefore evolution, of photonic scale structures. The first study by Wickham et al. (2006)
provided weak evidence7
to suggest that as simple optical structures, multilayer reflectors give rise to increasingly complex nano-architectures. This is through gradual optical refinement over time due to incremental changes in the genome. This theory presupposes that the evolution of simple reflectors is fully controlled by the random mutations of genes, which code for individual photonic structures. Wickham et al. (2006)
based their conclusions on an examination of multilayer reflectors in 10 unrelated species from the Nymphalidae and Papilionidae. Three types of reflector were recognized: untilted scute; untilted flute; and tilted scute (see previously f
for the first two types and (b
) for the third type). Simple and Dollo parsimony analyses showed that the untilted scute reflector (equivalent to a basic multilayer) was always at the base of the tree, suggesting that this represented the least-derived character state. The flute- and tilted scute multilayer structures evolved later, suggesting that they represent a more refined version of the untilted scute structure with a greater angle dependence and exaggeration of colour. These examples represent optical refinement for a specific optical function (assuming that this is the primary purpose of these nanostructures).
Wickham et al. (2006)
had followed a model where optical reflectors had been demonstrated to evolve by increasing complexity and optical efficiency in ostracods (Crustacea; Parker 1995
). However, in this case, the reflectors are formed by multiple cells contributing to the same optical structure, and optical improvements probably arose due to incremental changes in the genome, which led directly to incremental changes in chitin deposition. In butterflies, however, developmental studies have shown that individual scales (optical devices) originate from single cells (Overton 1966
Gradual increases in complexity over time are in line with traditional evolutionary theory and are based on the supposition that the genotype is proportional to the phenotype in the case of structural colours—multiple genes producing the complex scale architectures composed of multiple photonic structures, which give rise to different colours and effects. Indeed, something that emerges from Huxley's collection of electron micrographs is that the morphological plasticity of nanostructure is matched by that of the hues and intensities of colours and the visual effects produced by these simple photonic structures. However, there is an alternative explanation for how such architectural variation on the nanoscale may evolve.
In contrast to the conclusions of Wickham et al.'s (2006)
study, evidence from developmental observations suggests that control over the expression and evolution of simple and also complex photonic scale structures is not entirely genetic but may also involve self-assembly—the formation of a structure from components without the aid of enzymes, independent of the structure—and mechanical processes such as buckling, cracking or splitting (Ghiradella 1974
; Ghiradella & Radigan 1976
; Parker 2006
). Here, further formation of the structure's architecture takes place after protein biosynthesis from the ribonucleic acid.
Developmental studies of lepidopteran scales were first reported in the 1960s (e.g. Paweletz & Schlote 1964
; Overton 1966
; Greenstein 1972
). From this work, we know that basic (unspecialized) scales develop from scale cells, which extrude the cell membrane to form a sac—the rudimentary scale. Bundles of microfilaments assemble longitudinally around the inner surface of the cell membrane, intermittently forming regions of close contact with the membrane. Epicuticle is then extracellularly secreted onto the cell membrane. The longitudinal ridges subsequently develop between the microfilament bundles, which appear to behave as spacers. Procuticle is then deposited inside the epicuticle onto the ridges, leaving the regions between without the cuticle, which will later form windows into the lumen. Finally, the cell membrane withdraws and eventually dies back completely to leave the scale. Specialized scale photonic structures are then elaborations on this basic framework.
Ghiradella and her colleagues were the first to realize the potential importance of mechanical processes in photonic structural development, in studies of the simple multilayered UV-reflective scales of C. eurytheme
(Pieridae) males (Ghiradella 1974
; Ghiradella & Radigan 1976
). They suggested that the scutes were formed by a combination of elastic buckling of the ridge cuticle and tension exerted through contraction of the microfilaments (part of the cytoskeleton of the cell).
Later, self-assembly was also suggested by Ghiradella (1989)
to be involved in the formation of basic multilayer reflectors. Studies of C. ladon
(Lycaenidae) revealed that the contents of scale cells were arranged into pockets, between which ran fibrils and tubules of nascent cuticle, which appeared to be aligning themselves into stacks upon the ventral scale lamina. The fibrils and tubules eventually assembled to form the layers and spacers, separating adjacent layers.
Self-assembly has also been observed to occur with the addition of intracellular components of individual scale cells acting as templates (Ghiradella 1989
). This was reported during the development of complex three-dimensional polycrystalline structures (Ghiradella 1989
) in Mitoura grynea
(Lycaenidae). Tubular units were observed within the cytosol, which consisted of a membranous sleeve surrounding the nascent cuticle, termed membrane cuticle (MC) units. The sleeves appeared to be invaginations of the plasma membrane and therefore continuous extracellularly. These MC units self-assembled into clumps, packed in a face-centred cubic configuration, forming crystallites of the final lattice. Within each crystallite, the MC units enclosed tubules of smooth endoplasmic reticulum (SER), which was acting as a cuticular template. After approximately 2 days, the SER and the rest of the cell died back, leaving the completed lattice. Ghiradella (1989)
concluded from these observations that the three-dimensional lattice development was achieved by a combination of self-assembly of the MC units and SER templates. Although some aspects of the self-assembly templating and cracking and splitting processes will be under genetic control, the genotype does not directly determine the phenotype and hence we should not expect to find evolution via gradualism (Parker 2006
recently highlighted the similarities between photonic crystals (‘complex’ optical devices) across taxa and even kingdoms, showing that there are just four basic types (two-dimensional periodic stacks of (i) solid rods or (ii) hollow tubes (Parker et al. 2001
; Zi et al. 2003
) and three-dimensional (iii) opal or (iv) inverse opal (see Parker et al. 2003
; Biró et al. 2003
). All are morphologically very similar, consisting of components that are circular in cross section, though each is of variable dimensions. This suggests that intracellular structures, common to the general eukaryotic cell, may be employed in the manufacturing process (Parker 2006
), supporting the hypothesis proposed by Ghiradella (1989)
. It also suggests that the highly complex inverse opal-type structures could appear ‘suddenly’ in evolutionary time (without having to evolve stepwise). Developmental studies will prove crucial to this work in the future, having already shown that intracellular components of individual scale cells act as templates for some photonic structures (Overton 1966
; Ghiradella 1974
Huxley's collection reinforces Parker's (2006)
hypothesis, in that the inverse opal-type three-dimensional photonic crystals can be found in species of the butterfly orders Lycaenidae and the Papilionidae (Papilionidae) and also in the moths (Microlepidoptera). In comparing the closest living relatives of these species, no traces of potential ‘intermediate stages’, or phenotypic steps towards the inverse opal structure, were evident. Although this subject requires more attention, the evidence for intracellular-structure-assisted evolution of butterfly scale reflectors is strong.