A review of the diversity and evolution of photonic structures in butterflies, incorporating the work of John Huxley (The Natural History Museum, London from 1961 to 1990)

The photonic structures of butterfly wings are among the most anatomically diverse of all those in nature, giving rise to an unrivalled display of structural colours. These have recently become the focus of research by workers in a variety of disciplines, stimulated by their potential applications to technology ('biomimetics'). This interest, together with the discovery of unpublished electron micrographs taken by the late Dr John Huxley (Natural History Museum, London), prompted this review of butterfly photonics in general. The current work provides a synopsis of the literature to date, covering the diversity and evolution of these optical structures and incorporating Huxley's work, which represents an important biomimetic and evolutionary database on its own. This review deals with butterfly photonic devices according to the parts of the butterfly scales on which they occur. In this way, the information is ripe for evolutionary study.     

Structural colour and iridescence in plants: the poorly studied relations of pigment colour

Background

Colour is a consequence of the optical properties of an object and the visual system of the animal perceiving it. Colour is produced through chemical and structural means, but structural colour has been relatively poorly studied in plants.

Scope

This Botanical Briefing describes the mechanisms by which structures can produce colour. In plants, as in animals, the most common mechanisms are multilayers and diffraction gratings. The functions of structural colour are then discussed. In animals, these colours act primarily as signals between members of the same species, although they can also play roles in camouflaging animals from their predators. In plants, multilayers are found predominantly in shade-plant leaves, suggesting a role either in photoprotection or in optimizing capture of photosynthetically active light. Diffraction gratings may be a surprisingly common feature of petals, and recent work has shown that they can be used by bees as cues to identify rewarding flowers.

Conclusions

Structural colour may be surprisingly frequent in the plant kingdom, playing important roles alongside pigment colour. Much remains to be discovered about its distribution, development and function.     

Carotenoid‐based bill coloration functions as a social,not sexual,signal in songbirds (Aves: Passeriformes)

Many animals use coloration to communicate with other individuals. Although the signalling role of avian plumage colour is relatively well studied, there has been much less research on coloration in avian bare parts. However, bare parts could be highly informative signals as they can show rapid changes in coloration. We measured bill colour (a ubiquitous bare part) in over 1600 passerine species and tested whether interspecific variation in carotenoid‐based coloration is consistent with signalling to potential mates or signalling to potential rivals in a competitive context. Our results suggest that carotenoid bill coloration primarily evolved as a signal of dominance, as this type of coloration is more common in species that live in social groups in the nonbreeding season, and species that nest in colonies; two socio‐ecological conditions that promote frequent agonistic interactions with numerous and/or unfamiliar individuals. Additionally, our study suggests that carotenoid bill coloration is independent of the intensity of past sexual selection, as it is not related to either sexual dichromatism or sexual size dimorphism. These results pose a significant challenge to the conventional view that carotenoid‐based avian coloration has evolved as a developmentally costly, condition‐dependent sexual signal. We also suggest that bare part ornamentation may often signal different information than plumage ornaments.     

Ultraviolet and carotenoid‐based coloration in the viviparous lizard Zootoca vivipara (Squamata: Lacertidae) in relation to age,sex, and morphology

Lizards display structural and pigment‐based colorations, and their visual system is sensitive to wavelengths of 300–700 nm. However, few studies in squamate reptiles have quantified interindividual colour variation that includes the structural ultraviolet (UV) component (300–400 nm). In the present study, we investigated variability of a ventral UV/yellow–red ornamentation in the common lizard Zootoca vivipara, including an analysis of spatial distribution, as well as sex and age differences. We also investigated whether the expression of coloration is related to body size and condition. Our analyses revealed two distinct patches: a gular patch with a strong UV reflectance and a belly patch with a dominant yellow–red reflectance. Males displayed a less saturated throat coloration with higher UV chroma and UV hue, and had a redder but duller belly coloration than females. Yearlings had less elaborate ornaments than adults, although they already displayed a yellow–red sexual dichromatism on the belly. UV sexual dichromatism was only apparent in adults as a result of a weaker UV reflectance in females, suggesting potential fitness costs of a bright UV coloration in that sex. Different colour traits were related to body size in both sexes, as well as to body condition in males. We discuss the potential evolutionary scenarios leading to the maintenance of this ornament in common lizards. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 128–141.     

Clutch size manipulations in the chestnut weevil, Curculio elephas: fitness of oviposition strategies

We test the adaptive value of clutch size observed in a natural population of the chestnut weevil Curculio elephas. Clutch size is defined as the number of immatures per infested chestnut. In natural conditions, clutch size averages 1.7 eggs. By manipulating clutch size in the field, we demonstrate that deviations from the theoretical ”Lack clutch size”, estimated as eight immatures, are mainly due to proximate and delayed effects of clutch size on offspring performance. We show the existence of a trade-off between clutch size and larval weight. The latter, a key life-history trait, is highly correlated with fitness because it is a strong determinant of larval survival and potential fecundity of offspring females. The fitness of different potential oviposition strategies characterized by their clutch sizes, ranging from one to nine immatures, was calculated from field- estimated parameters. Chestnut weevil females obtain an evolutionary advantage by laying their eggs singly, since, for instance, fitness of single-egg clutches exceeds fitness of two-egg clutches and four-egg clutches by 8.0% and 15.1% respectively. Received 4 August 1999 / Accepted: 7 October 1999     

Habitat heterogeneity, predation and gene flow: colour polymorphism in the isopod, Idotea baltica

The colour polymorphic isopod Idotea baltica inhabits the brown alga Fucus vesiculosus which is often colonised by the white epizoite Electra crustulenta (Bryozoa). In an experiment the predation risk for the different colour morphs of I. baltica was highly dependent on background colouration. Morph frequencies and Electra density varied substantially among 10 collecting sites but correlated poorly with each other, suggesting that local selection for cryptic colouration may be counteracted by gene flow. Indeed, estimates based on four polymorphic allozymes suggested rate of gene flow to be high. These results support the hypothesis that locally varying selection for cryptic colouration counteracted by gene flow contributes to the maintenance of colour polymorphism in I. baltica. The visual differences between the microhabitats and the differential microhabitat use between males and females seem to result in different patterns of selection on males and females for cryptic colouration. Also this is likely to play an important role for the polymorphism.     

Iridescent ultraviolet signal in the orange sulphur butterfly (Colias eurytheme): spatial, temporal and spectral properties

Many of nature's most striking animal colours are iridescent, exhibiting a high degree of spectral purity and strong angular dependence of intensity and hue. Although a growing number of studies have detailed the intricate mechanisms responsible for producing iridescent colours, few attempts have been made to describe their dynamic appearance in ecologically and behaviourally realistic contexts. We suggest that the optical properties unique to iridescent structural colours are important for understanding how they function as signals during behavioural interactions. Using males of the orange sulphur butterfly, Colias eurytheme , which exhibit an iridescent ultraviolet (UV) reflectance on their dorsal wing surfaces, we develop a holistic framework for inferring the appearance of this signal to conspecifics under field conditions that incorporate data on their spectral sensitivity. We show that, during flight, the UV signal is brightest within a wing beat cycle when viewed from directly above the male. Spectral properties of the signal under natural lighting indicate that male wing colour should be readily perceived and distinguished from that of females and from the dark green visual background of UV-absorbing vegetation. Finally, our analyses permit predictions regarding how signal senders and receivers should orientate themselves for maximal transmission and reception of this ultraviolet iridescent signal.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 349–364.     

Microstructure of mandibulate mouthparts in the greater rice weevil,Sitophilus zeamais (Coleoptera: Curculionidae)

The greater rice weevil, Sitophilus zeamais, is a serious pest of stored grain. It chews a hole in the grain and deposits an egg inside. For the purpose of excavating a tunnel, these weevils are equipped with effective mandibulate mouthparts for penetrating and boring holes. The mouthparts of the weevil are a long slender snout, which consist of a labrum, a pair of mandibles, a pair of maxillae and a labium. Mothparts exhibit typical morphology of phytophagous coleopteran beetles and have characteristics of chewing mouthparts. Mandibles are connected to the head capsule through dicondyous articulation, which allows movement along one single rotating axis. Both labrum and labium are fused to the snout and form the upper and lower lips, respectively. Along the depressed surface of the snout, a number of short sensory hairs are sparsely arranged. The distal apexes of the maxillary and labial palpi are deeply depressed into a sensillar field, and only one type of the basiconic sensilla, which function as chemo‐ or gustatory receptors, occurs in both sexes.     

Proteolytic gut activities in the rice water weevil,Lissorhoptrus brevirostris Suffrian (Coleoptera: Curculionidae)

Digestive endoprotease activities of the rice water weevil, Lissorhoptrus brevirostris Suffrian (Coleoptera: Curculionidae), were characterized based on the ability of gut extracts to hydrolyze specific synthetic substrates, optimal pH, and hydrolysis sensitivity to protease inhibitors. Larvae of this species were found to use a complex proteolytic system that includes cathepsin D-, cathepsin B-, trypsin-, and chymotrypsin-like activities. Trypsin-like activity was evenly distributed among the anterior, middle, and posterior portions of the gut, whereas cathepsin B- and cathepsin D-like activities were mainly located in the anterior and middle sections, and the chymotrypsin-like activity was highest in the middle and posterior sections. Gelatin-containing native-PAGE gels indicated the presence of several aspartyl, cysteine, and serine protease forms and confirmed the spatial organization of the proteolytic digestive process.     

Latitudinal variation of morphological characteristics in the swallowtail Sericinus montelus Gray, 1798 (Lepidoptera: Papilionidae)

Patterns of latitudinal variation in the phenotype or genotype of an organism may provide evidence for natural selection. In this study, we investigated seven populations of swallowtail Sericinus montelus Gray, 1798 (Lepidoptera: Papilionidae), a non‐migratory species, to explore the latitudinal variation of morphological characteristics in adults. The results showed that body size and the development of dark pigmentation on wings in this species responded strongly to latitude. The body size of both male and female adult of S. montelus was negatively correlated with latitude. These findings provided solid evidence to support the converse Bergmann's rule. We considered that the observed variation in morphological characteristics was most likely mediated by the seasonal length and thermoperiod to adapt to different latitudinal environment (e.g. shortened developmental time of immature stages for smaller body size at higher latitude). Moreover, the tendency towards progressively darker colour patterns (only in adult males) at increasingly low latitudes was consistent with Gloger's rule. We suggested that the observed colour variation was most likely associated with thermoregulation. Slight variation in the morphology of the W‐shaped stripe on the forewing of adult females was also found, and we presumed that the functions of sexual preferences, mimicry and thermoregulation might be involved.     

Characterization of microsatellite loci in Brachyderes rugatus,the Canary Islands pine weevil (Coleoptera: Curculionidae)

The Canary Island pine weevil Brachyderes rugatus (Wollaston) consists of four allopatric subspecies that are thought to have arisen from several historic colonization events within the archipelago. We have isolated and optimized seven microsatellite loci from Brachyderes rugatus calvus from Gran Canaria. Six of these loci are polymorphic within B. rugatus (11–22 alleles per locus; heterozygosity between 0.43 and 0.84). There is no evidence for heterozygote deficit within populations or for linkage disequilibrium between pairs of loci. These molecular markers are likely to prove useful tools for quantifying the genetic variability of bottlenecked island populations.     

Rhabdom evolution in butterflies: insights from the uniquely tiered and heterogeneous ommatidia of the Glacial Apollo butterfly, Parnassius glacialis

The eye of the Glacial Apollo butterfly, Parnassius glacialis, a 'living fossil' species of the family Papilionidae, contains three types of spectrally heterogeneous ommatidia. Electron microscopy reveals that the Apollo rhabdom is tiered. The distal tier is composed exclusively of photoreceptors expressing opsins of ultraviolet or blue-absorbing visual pigments, and the proximal tier consists of photoreceptors expressing opsins of green or red-absorbing visual pigments. This organization is unique because the distal tier of other known butterflies contains two green-sensitive photoreceptors, which probably function in improving spatial and/or motion vision. Interspecific comparison suggests that the Apollo rhabdom retains an ancestral tiered pattern with some modification to enhance its colour vision towards the long-wavelength region of the spectrum.     

Efficacy of cashew kernel extracts in the control of the maize weevil,Sitophilus zeamais (Coleoptera: Curculionidae)

Six different solvents namely: methanol, ethanol, water, acetone, pet-ether or n-hexane was used to extract the essential oils from cashew kernel. The extracted oils were evaluated on Sitophilus zeamais (Motschulsky 1855) for mortality, oviposition and adult emergence effects. The long-term storage and water absorption capacity of the treated maize grains was also investigated. Results showed that the steam distillate was most lethal on S. zeamais. The least potent extracts on S. zeamais were those extracted with methanol and ethanol. The extracts drastically reduced oviposition in S. zeamais. Maize grains treated with steam distillate extract had the lowest water absorption capacity, while the highest water absorption capacity was obtained in grains treated with ethanol and methanol. Extracts of steam distillate, n-hexane, petroleum ether and acetone completely prevented infestation and subsequence damage of the treated maize grains for a period of three months. In the grains treated with the methanol and ethanol extracts, damage of 28.61% and 6.24%, respectively were obtained. The results obtained reveal that extracts of cashew kernel are effective in controlling S. zeamais and could serve as an alternative to synthetic insecticides.     

Natural selection and the distribution of shell colour morphs in three species of Littoraria (Gastropoda: Littorinidae) in Moreton Bay, Queensland

The distribution of yellow, brown and red morphs of sympatric species of Littoraria were recorded on mangrove trees of the genus Avicennia within Moreton Bay, Queensland. The roles of background mimicry (leaf vs. bark, dark vs. light), niche selection and thermal tolerance (sunny vs. shaded positions and height above ground) were examined. The yellow advantage found previously in the area was tested. Total yellow morph frequency adjusted to a reduction in leaf background on pruned trees. Morph frequencies in Littoraria species reflect differences in habitat use. L. filosa (high yellow frequency) was more frequently found on leaves at the highest tree levels, while L. luteola (high brown frequency) was more frequently found on branches at lower levels. It is therefore argued that morphs mimic background elements. Previously reported niche selection by yellow and brown morphs of leaf and bark backgrounds is shown to be a result of the distribution of L. luteola on branches and L. filosa on leaves. At warmer times of the year, yellow L. filosa were more common in sunny positions; this is thought to be a result of thermal tolerance. There appears to be some advantage to particular morphs on particular tree types, but this relationship needs to be examined further. Mangrove-dwelling Littoraria are a promising model to investigate molluscan polymorphism. In the past, erroneous identification of sympatric species may have influenced the accuracy of reported patterns. We used allozyme electrophoretic markers as a precise identification technique. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 75 , 219–232.     

Geographic variation in the long-nosed snake, Rhinocheilus lecontei (Colubridae): beyond the subspecies debate

Scalation, colour pattern, linear and geometric morphometrics were used to quantify geographical differentiation in the long-nosed snake, Rhinocheilus lecontei, and to test the hypothesis that all four subspecies are morphologically distinct. Also investigated were potential associations between morphological (scalation, colour pattern, linear measurements) and environmental variables (climate, vegetation, soil). Sexual dimorphism was weakest for geometric and strongest for linear morphometric variables. Morphological variables differed widely in their ability to differentiate subspecies. Linear morphometric variables achieved the most statistically significant pairwise Mahalanobis distances between subspecies, while geometric morphometrics largely failed to differentiate them. Colour pattern showed the strongest and linear morphometrics the weakest correlation with environment. Several characters varied continuously along latitudinal or longitudinal gradients, such that, in some cases, the clines for closely related traits were discordant. No one subspecies was consistently divergent in all analyses, leading to the conclusion that the three mainland subspecies are not sufficiently distinct to warrant separate subspecies status. The island subspecies, though not always statistically distinct, is geographically separate from other populations and differs in characters related to size. Given the small number of specimens available, a decision regarding its taxonomic status (i.e. elevation to species level) is best deferred until additional specimens can be examined and data on molecular variation can be analysed.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 65–85.     

Effects of temperature on the expression of elytral colour polymorphism in the ladybird beetle,Menochilus sexmaculatus (Coleoptera: Coccinellidae)

The ladybird beetle, Menochilus sexmaculatus (Fabricius), has a remarkable elytral colour polymorphism composed of black and red. In the present study, we investigated the effect of temperature on growth from the first instar larva to the pupal stage, as well as maternal morph types on the phenotypic expression of the elytral colour morph in a polymorphic population from Osaka, Japan. Female individuals of three different elytral colour morphs were collected from a wild population, and hatchlings from each female were divided into three groups, which were reared at three constant temperatures: 20 °C, 25 °C, and 30 °C. The phenotypic frequency of F₁ adults indicated that the elytral morph type was determined by genetic factors, but not by growth temperatures. Namely, type A (almost black morph) was the most abundant in F₁ from type A mothers (Male: 52.6%; Female: 32.3%); and types B (four small-dotted morph) and F (four medium-dotted morph) were the most abundant from type B (Male: 56.7%; Female: 53.3%) and type G (four larger-dotted morph) mothers (Male: 33.3%; Female: 31.3%), respectively. Therefore, the expression of elytral colour polymorphism in the Osaka, Japan population is likely to have a genetic basis contingent on parental morphs, rather than a phenotypic plasticity associated with growth temperatures.     

Long-term variation in colour-morph frequencies in the spider Enoplognatha ovata (Glerck) (Araneae: Theridiidae): natural selection, migration and intermittent drift

The spider Enoplognatha ovata is univoltine. It has three principal visible morphs, lineata, redimita and mala , whose genetics are understood. Phenotype frequencies and population sizes have been estimated at 44 sites in a single valley in Yorkshire for periods of up to 15 years. Geographically, recognizable areas of high and low frequencies of redimita and ovata are found, typically a few hundred metres across. Statistically significant frequency differences also exist on a scale of tens of metres between adjacent sites. Temporal variation in lineata allele frequency has been investigated using a weighted regression technique assuming either no deterministic change or a steady change at constant rate. There is little direct evidence for selection but variation within sites is less than would be expected through genetic drift. A negative relationship is demonstrated between initial allele frequency in a site and the direction and rate of allele frequency change with time, suggesting that populations are moving towards a global equilibrium. This conclusion is insensitive to varying assumptions about the relationship between estimated and effective population sizes. Evidence from transplantation experiments and from the most isolated site indicate that both migration and selection contribute to this trend. We suggest that populations were stochastically perturbed from the equilibrium during bottlenecks in population size which resulted from major habitat disturbance about 35 years ago.     

Adaptive plasticity of egg size in response to competition in the cowpea weevil,Callosobruchus maculatus (Coleoptera: Bruchidae)

Life history theory predicts that larger propagules should be produced when the offspring are expected to experience intense competition. This study tested whether female cowpea weevils responded to high larval or adult density by producing larger eggs. In a splitbrood design I measured the effect of density experienced by females at their larval stage (1 vs. 4–6 larvae/cowpea) on the size of eggs produced just after emergence. The females were then kept either at low adult density (1 female+1 male per vial), or at high adult density (10 females+10 males) for 2 days, and tested for the effect of this adult density treatment on the size of eggs laid subsequently. I measured egg length and width, as well as the diameter of the entrance tunnel made by the larva, which can be regarded as a crude measure of larval size. Females that experienced high adult density subsequently laid slightly wider eggs than those kept at low density. This difference, albeit small (about 1–4% after correction for female weight and the effect of family, depending on the statistical model used), was statistically significant and robust to alterations of the statistical model. It may be a remnant of a larger plastic response of egg size to competition that has become eroded during many generations in high-density laboratory cultures. There was no difference in egg length or the diameter of the entrance tunnel. Eggs laid just after emergence by females reared at high larval density also tended to be wider than those produced by females that had no competitors. This effect was only marginally significant, however, and sensitive to the statistical model. Both egg length and width and the diameter of the entrance tunnel increased with female weight and decreased with female age. The tunnel diameter was positively correlated with both egg length and width, but the effect of width was larger.