Butterfly wings: Colour patterns and now gene expression patterns

The particular fascination of butterfly wings for developmental biologists (and others) lies in their spectacular array of colour patterns. The evolutionary and developmental relationships between these patterns have been analysed and we know something of the cell interactions involved in their formation⁽¹⁾. Now butterfly homologues of Drosophila wing-patterning genes have been identified, and their expression patterns offer the first clues to the molecular mechanisms which specify wing colour patterns⁽²⁾.     

Adaptive evolution of facial colour patterns in Neotropical primates

The rich diversity of primate faces has interested naturalists for over a century. Researchers have long proposed that social behaviours have shaped the evolution of primate facial diversity. However, the primate face constitutes a unique structure where the diverse and potentially competing functions of communication, ecology and physiology intersect, and the major determinants of facial diversity remain poorly understood. Here, we provide the first evidence for an adaptive role of facial colour patterns and pigmentation within Neotropical primates. Consistent with the hypothesis that facial patterns function in communication and species recognition, we find that species living in smaller groups and in sympatry with a higher number of congener species have evolved more complex patterns of facial colour. The evolution of facial pigmentation and hair length is linked to ecological factors, and ecogeographical rules related to UV radiation and thermoregulation are met by some facial regions. Our results demonstrate the interaction of behavioural and ecological factors in shaping one of the most outstanding facial diversities of any mammalian lineage.     

Butterfly wing colours: scale beads make white pierid wings brighter

The wing-scale morphologies of the pierid butterflies Pieris rapae (small white) and Delias nigrina (common jezabel), and the heliconine Heliconius melpomene are compared and related to the wing-reflectance spectra. Light scattering at the wing scales determines the wing reflectance, but when the scales contain an absorbing pigment, reflectance is suppressed in the absorption wavelength range of the pigment. The reflectance of the white wing areas of P. rapae, where the scales are studded with beads, is considerably higher than that of the white wing areas of H. melpomene, which has scales lacking beads. The beads presumably cause the distinct matt-white colour of the wings of pierids and function to increase the reflectance amplitude. This will improve the visual discrimination between conspecific males and females.     

Butterfly wing patterns

This paper integrates genetical studies of variation in the wing patterns of Lepidoptera with experimental investigations of developmental mechanisms. Research on the tropical butterfly,Bicyclus anynana, is described. This work includes artificial selection of lines with different patterns of wing eyespots followed by grafting experiments on the lines to examine the phenotypic and genetic differences in terms of developmental mechanisms. The results are used to show how constraints on the evolution of this wing pattern may be related to the developmental organisation. The eyespot pattrn can be envisaged as a set of developmental homologues; a common developmental mechanism is associated with a quantitative genetic system involving high genetic correlations. However, individual genes which influence only subsets of the eyespots, thus uncoupling the interdependence of the eyespots, may be important in evolutionary change. The postulated evolutionary constraints are illustrated with respect to differences in wing pattern found among other species ofBicyclus.     

The evolution of hymenopteran wings: the importance of size

The allometric relationships between body size and several aspects of wing morphology in the insect order Hymenoptera were investigated using multivariate morphometric techniques. The study focused primarily on wing allometry in five monophyletic genera of bees ( Perdila, Halictus, Ceratina, Trigona and Apis ), but the patterns of size-related evolutionary change found within each of these genera are also found to exist in numerous other hymenopteran taxa. Increased body size in hymenopteran lineages is correlated with the following changes in wing morphology: (1) decreased relative stigma area, (2) distal extension of wing vein elements, (3) increased aspect ratio and (4) proximal shift in the centroid of wing area. The reverse is true for decreased size. The widespread allometric trends most likely result from adaptive change in wing morphology due to size-related changes in the physical properties impinging on the organism–principally the quality and magnitude of drag. The fact that similar wing morphologies among distantly related species can result from similarity in body size has important implications for the study of hymenopteran phylogeny, especially at lower taxonomic levels and when a high proportion of wing characters are employed.     

Towards a theory of the evolution of butterfly colour patterns under directional and disruptive selection

Two general models for the transspecific evolution of butterfly colour patterns are advanced: directional selection acting equally on both sexes, and disruptive selection involving periods of polymorphism. To consider possible outcomes of me latter process, a morphism notation based on an integrated classification for polymorphism and sexual dimorphism is developed. This notation is used to examine the properties of all morphism transformations possible from the minimal expressions of the nine morphism categories, as reached through defined minimum step changes. The significance of such pathway models is analysed in terms of general properties of butterfly polymorphism. The potential use of pathway models in evolutionary studies is briefly discussed, mainly with respect to phylogenetics, and ideas on the evolution of genetic dominance.     

Factors shaping the evolution of colour patterns in Australian agamid lizards (Agamidae): a comparative study

Identifying general patterns of adaptive coloration in animals can help to elucidate the evolutionary processes that generate them. We examined the evolution of colour patterns in Australian agamid lizards, a morphologically and ecologically diverse group that relies primarily on visual communication. We tested whether certain types of colour (yellow–reds and black) were likely to be used as sexual signals, as indicated by their association with indices of sexual selection, namely, sexual dichromatism and sexual dimorphism in body size and head shape. We then tested whether sexually dichromatic colours are associated with specific patterns (uniform, mottled, striped, blotched, reticulated) or ecological variables such as habitat openness, arboreality, and substrate type. The presence of yellow–red on lateral and ventral body regions and black on ventral body regions was significantly more common in males than females. Lateral yellow–red in males was associated with the total extent of sexual dichromatism and size dimorphism, whereas ventral yellow–red was associated with sexual dichromatism. Both lateral and ventral yellow–red were associated with uniform patterning, suggesting that sexual signals in male agamid lizards may often comprise uniform patches or flushes of yellow–red. Although ventral black coloration was more prevalent on males (i.e. strongly sexually dichromatic), it was not associated with indices of sexual selection, suggesting that, in agamid lizards, yellow–red coloration is more likely to be sexually selected than black. Sexually dichromatic coloration was not strongly associated with any of the ecological variables measured. We found some associations, however, between female dorsal patterns and ecological variables, suggesting that female patterns are influenced by natural selection. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 101–112.     

Origin and development of the wings of Lepidoptera

Summary In Lepidoptera (Pieris rapae) the imaginal wing discs originate by a thickening of the thoracic pleural hypodermis at the close of embryonic life. The tracheoles originate in the endotracheal layer at the close of the first moult and become functional at the close of second moult. They grow very rapidly and reach their limit of penetration in the larval wing at end of third moult. At the beginning of fifth instar they become less abundant degenerate and disappear by absorption in the pupal wing.The permanent system of tracheoles evaginate from the wing trachea in the prepupal stage and become functional during pupal life. The wing passes to the exterior by a drawing back of the hypodermal wing sac. The rapid expansion of the wing causes the withdrawal of hypodermis. The sharp division into larval and pupal stages applies more particularly to the exterior of the body as they follow one another after successive moults, the internal development is a continuous series of transformations, between which there is no sharp line of demarcation. Yet on the whole the form of larva, pupa and imago are kept distinct in adaptation to their separate environments and habits.

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Zusammenfassung Die imaginalen Flügelscheiben nehmen bei Schmetterlingen (Pieris rapae) ihren Ursprung ans einer Verdickung der pleuralen Thoraxhypodermis am Schlusse des Embryonallebens. Die Tracheolen nehmen ihren Ursprung in der endotrachealen Schicht am Schlusse der ersten Häutung und beginnen am Schlusse der zweiten zu funktionieren. Sie wachsen sehr rasch und erreichen die Grenze ihres Eindringens in den Larvenflügel am Ende der dritten Häutung. Am Beginne der fünften werden sie dagegen weniger reichlich, degenerieren und verschwinden durch Absorption im Flügel der Puppe.Das bleibende Tracheolensystem stülpt sich aus der Flügeltrachea im Vorpuppenstadium aus und tritt während des Puppenlebens in Funktion. Der Flügel gelangt durch ein Zurückziehen des hypodermalen Flügelsackes an die Außenwelt. Die rapide Ausdehnung des Flügels veranlaßt das Zurückweichen der Hypodermis. Die scharfe Teilung in Larven- und Puppenstadium findet ihre Anwendung mehr auf das Körperäußere, da das eine auf das andre nach successiven Häutungen folgt. Die innere Entwicklung ist eine kontinuierliche Reihe von Formveränderungen, zwischen denen keine scharfe Trennungslinie existiert. Im ganzen aber bleiben die Larven-, Puppen- und Imagoform je nach Anpassung an ihre verschiedene Umgebung und ihre verschiedenen Lebensgewohnheiten streng getrennt.

     

The development and evolution of bristle patterns in Diptera

The spatial distribution of sensory bristles on the notum of different species of Diptera is compared. Species displaying ancestral features have a simple organization of randomly distributed, but uniformly spaced, bristles, whereas species thought to be more derived bear patterns in which the bristles are aligned into longitudinal rows. The number of rows of large bristles on the scutum was probably restricted to four early on in the evolution of cyclorraphous Brachyceran flies. Most species have stereotyped patterns based on modifications of these four rows. The possible constraints placed upon the patterning mechanisms due to growth and moulting within the Diptera are discussed, as well as within hemimetabolous insects. The holometabolic life cycle and the setting aside of groups of imaginal cells whose function is not required during the growth period, may have provided the freedom necessary for the evolution of elaborate bristle patterns. We briefly review the current state of knowledge concerning the complex genetic pathways regulating achaete-scute gene expression and bristle pattern in Drosophila melanogaster, and consider mechanisms for the genetic regulation of the bristle patterns of other species of Diptera.     

New evidence for parallel evolution of colour patterns in Malagasy poison frogs (Mantella)

Malagasy poison frogs of the genus Mantella are diurnal and toxic amphibians of highly variable and largely aposematic coloration. Previous studies provided evidence for several instances of homoplastic colour evolution in this genus but were unable to sufficiently resolve relationships among major species groups or to clarify the phylogenetic position of several crucial taxa. Here, we provide cytochrome b data for 143 individuals of three species in the Mantella madagascariensis group, including four newly discovered populations. Three of these new populations are characterized by highly variable coloration and patterns but showed no conspicuous increase of haplotype diversity which would be expected under a scenario of secondary hybridization or admixture of chromatically uniform populations. Several populations of these variable forms and of M. crocea were geographically interspersed between the distribution areas of Mantella aurantiaca and Mantella milotympanum. This provides further support for the hypothesis that the largely similar uniformly orange colour of the last two species evolved in parallel. Phylogenies based on over 2000 bp of two nuclear genes (Rag-1 and Rag-2) identified reliably a clade of the Mantella betsileo and Mantella laevigata groups as sister lineage to the M. madagascariensis group, but did not support species within the latter group as monophyletic. The evolutionary history of these frogs might have been characterized by fast and recurrent evolution of colour patterns, possibly triggered by strong selection pressures and mimicry effects, being too complex to be represented by simple bifurcating models of phylogenetic reconstruction.     

On the measurement and classification of colour in studies of animal colour patterns

In studies of animal colouration it is no longer necessary to rely on subjective assessments of colour and conspicuousness, nor on methods which rely upon human vision. This is important because animals vary greatly in colour vision and colour is context-dependent. New methods make it practical to measure the colour spectrum of pattern elements (patches) of animals and their visual backgrounds for the conditions under which patch spectra reach the conspecific's, predator's or prey's eyes. These methods can be used in both terrestrial and aquatic habitats. A patch's colour is dependent not only upon its reflectance spectrum, but also upon the ambient light spectrum, the transmission properties of air or water, and the veiling light spectrum. These factors change with time of day, weather, season and microhabitat, so colours must be measured under the conditions prevalent when colour patterns are normally used. Methods of measuring, classifying and comparing colours are presented, as well as techniques for assessing the conspicuousness of colour patterns as a whole. Some implications of the effect of environmental light and vision are also discussed.     

Design, function and evolution in the wings of holometabolous insects

The wings of Holometabola are reviewed in functional terms. Two basic types, anteroposteriorly symmetric ('symmetric') and anteroposteriorly asymmetric ('asymmetric'), are recognized and their modes of operation discussed. Most neuropteroids have asymmetric wings, whereas relative anteroposterior symmetry appears plesiomorphic for mecopteroids. Wing coupling has only occurred in lineages with wings of symmetric type, but anteroposterior asymmetry of the wing couple has later developed several times in association with improved, more versatile, flight performance. Coleoptera wings seem to have developed from predecessors of symmetric type, but their morphology is strongly influenced by the need to fold up at rest. Diptera provide an excellent illustration of the evolution of asymmetric, high-performance wings from the symmetric, 'mecopteran' type. Asymmetric and symmetric wings can both be derived from less specialized types. Both are well represented as fossils from the Permian onwards, and these supply further examples of the evolution of asymmetry from the symmetric pattern.     

A molecular phylogenetic analysis of the pleasing fungus beetles (Coleoptera: Erotylidae): evolution of colour patterns, gregariousness and mycophagy

Abstract. Phylogenetic relationships of Erotylidae (pleasing fungus beetles) were inferred based on DNA sequence data. Relationships of clades within Erotylidae were examined, as was the relationship of the entire family to Languriidae (lizard beetles). 18S and 28S ribosomal DNA were sequenced for sixty‐one taxa representing major erotylid lineages and outgroups. Phylogenetic analyses under varying parameter settings using standard parsimony and likelihood techniques were performed. These data indicate a paraphyletic Erotylidae and Languriidae. Encaustinae (including Coptengis), Megalodacninae and Erotylinae are supported as monophyletic, whereas Dacninae and Tritominae are paraphyletic. Taxonomic and biological implications are discussed. Gregariousness has arisen at least three times in Erotylidae. The erotylid clade has experienced at least one evolutionary transition from mycophagy (on Aphyllophorales) to phytophagy, three transitions from Aphyllophorales hosts to Euagarics, and one transition from Euagarics hosts to Mucorales (Zygomycetes). There are no recognizable phylogenetic trends in coloration across higher‐level erotylid lineages.     

The colour patterns of cypraeid gastropods

Colour patterns on mollusc shells are usually controlled by one-dimensional morphogenetic programmes. In adult cypraeids, by comparison, colour patterns are two-dimensional in morphogenesis and three-dimensional in structure. Visible patterns usually result from the uneven thickness of a pigmented layer, rather than from a spatially uneven concentration of pigment. Specialized sculptures in a few cypraeids may be regarded as extreme examples of three-dimensional colour patterns. Morphogenesis of some patterns is controlled by three-dimensional relief of the underlying shell surface. Computer models successfully reproduce key characteristics of cypraeid colour patterns. Since most cypraeids possess colour patterns, while few of the combinations of factors controlling these programmes yield a pattern, these patterns can be expected to have a yet undemonstrated adaptive value.     

Evolutionary genetics: the evolution of plumage patterns

The identification and sequencing of a gene affecting melanin production in the bananaquit, a bird species notable for its polymorphic plumage colour, paves the way for much greater understanding of the evolution of plumage patterns in birds, and the developmental modulations involved in producing new patterns.     

Left-right asymmetry of fly wings and the evolution of body axes.

The body plan of Drosophila, and presumably that of other insects, develops under the control of anterio-posterior and dorsal ventral axes, but no evidence for a left-right axis has yet been found. We used geometric morphometrics to study the wings in three species of flies: Drosophila melanogaster, Musca domestica and Glossina palpalis gambiensis. In all three species, we found that both size and shape showed subtle, but statistically significant directional asymmetry. For size, these asymmetries were somewhat inconsistent within and between species, but for shape, highly significant directional asymmetry was found in all samples examined. These systematic left-right differences imply the existence of a left-right axis that conveys distinct positional identities to the wing imaginal discs on either body side. Hence, the wing discs of Drosophila may be a new model to study the developmental genetics of left-right asymmetry. The asymmetries of shape were similar among species, suggesting that directional asymmetry has been evolutionarily conserved since the three lineages diverged. We discuss the implications of this evolutionary conservatism in conjunction with results from earlier studies that showed a lack of genetic variation for directional asymmetry in Drosophila.